Mechanisms of vascular calcification in CKD - Evidence for premature ageing?

Nature Reviews Nephrology

Volumn 9, Issue 11, 2013, Pages 661-670

  Shanahan, Catherine M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ATM PROTEIN; ATR PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; FETUIN A; FIBROBLAST GROWTH FACTOR 23; INTERLEUKIN 6; KLOTHO PROTEIN; LAMIN A; OSTEOCALCIN; OSTEOPROTEGERIN; PRELAMIN A; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; UREMIC TOXIN;

APOPTOSIS; BLOOD VESSEL CALCIFICATION; BONE DEVELOPMENT; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CELL AGING; CELL DIFFERENTIATION; CHRONIC KIDNEY DISEASE; DNA DAMAGE; HEMODIALYSIS PATIENT; HUMAN; METABOLIC REGULATION; MINERAL METABOLISM; NONHUMAN; NUCLEAR LAMINA; OXIDATIVE STRESS; PHENOTYPE; PREMATURE AGING; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; VASCULAR SMOOTH MUSCLE;

AGING; AGING, PREMATURE; HUMANS; RENAL INSUFFICIENCY, CHRONIC; RISK FACTORS; VASCULAR CALCIFICATION;

EID: 84890806053     PISSN: 17595061     EISSN: 1759507X     Source Type: Journal    
DOI: 10.1038/nrneph.2013.176     Document Type: Review

References (123)

1. Go, A. S. et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 351, 1296-1305 (2004).
2. Goodman, W. G. et al. Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N. Engl. J. Med. 342, 1478-1483 (2000).
3. Foley, R. N. & Parfrey, P. S. Cardiovascular disease and mortality in ESRD. J. Nephrol. 11, 239-245 (1998).
4. Mitsnefes, M. M. Cardiovascular disease in children with chronic kidney disease. J. Am. Soc. Nephrol. 23, 578-585 (2012).
5. Virchow, R. Cellular pathology. As based upon physiological and pathological histology. Lecture XVI-Atheromatous affection of arteries. 1858. Nutr. Rev. 47, 23-25 (1989).
6. McEniery, C. M. et al. The impact of cardiovascular risk factors on aortic stiffness and wave reflections depends on age: The Anglo-Cardiff Collaborative Trial (ACCT III). Hypertension 56, 591-597 (2010).
7. Kovacic, J. C. et al. Cellular senescence, vascular disease, and aging: Part 1 of a 2 part review. Circulation 123, 1650-1660 (2011).
8. Kovacic, J. C. et al. Cellular senescence, vascular disease, and aging: Part 2 of a 2 part review: Clinical vascular disease in the elderly. Circulation 123, 1900-1910 (2011).
9. London, G. M. Arterial calcification: Cardiovascular function and clinical outcome. Nefrologia 31, 644-647 (2011).
10. London, G. M. et al. Arteriosclerosis, vascular calcifications and cardiovascular disease in uremia. Curr. Opin. Nephrol. Hypertens. 14, 525-531 (2005).
11. Shaw, L. J. et al. Coronary artery calcium as a measure of biologic age. Atherosclerosis 188, 112-119 (2006).
12. Girndt, M. & Seibert, E. Premature cardiovascular disease in chronic renal failure (CRF): A model for an advanced ageing process. Exp. Gerontol. 45, 797-800 (2010).
13. Block, G. A. et al. Association of serum phosphorus and calcium x phosphate product with mortality risk in chronic hemodialysis patients: A national study. Am. J. Kidney Dis. 31, 607-617 (1998).
14. Tonelli, M. et al. Relation between alkaline phosphatase, serum phosphate, and all-cause or cardiovascular mortality. Circulation 120, 1784-1792 (2009).
15. London, G. M. Bone-vascular cross-talk. J. Nephrol. 25, 619-625 (2012).
16. Mackenzie, I. S. et al. Comparison of the effects of antihypertensive agents on central blood pressure and arterial stiffness in isolated systolic hypertension. Hypertension 54, 409-413 (2009).
17. Wanner, C. et al. Atorvastatin in patients with type 2 diabetes mellitus undergoing hemodialysis. N. Engl. J. Med. 353, 238-248 (2005).
18. Shanahan, C. M. et al. Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: Evidence for smooth muscle cell-mediated vascular calcification. Circulation 100, 2168-2176 (1999).
19. Shroff, R., Long, D. A. & Shanahan, C. Mechanistic insights into vascular calcification in CKD. J. Am. Soc. Nephrol. 24, 179-189 (2013).
20. Liu, Y. et al. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence associated secretory phenotype in vascular smooth muscle cells. Circ. Res. 112, e99-e109 (2013).
21. Nakano-Kurimoto, R. et al. Replicative senescence of vascular smooth muscle cells enhances the calcification through initiating the osteoblastic transition. Am. J. Physiol. Heart Circ. Physiol. 297, H1673-H1684 (2009).
22. Marchand, A. et al. The Wnt/beta-catenin pathway is activated during advanced arterial aging in humans. Aging Cell 10, 220-232 (2011).
23. Burton, D. G. et al. Microarray analysis of senescent vascular smooth muscle cells: A link to atherosclerosis and vascular calcification. Exp. Gerontol. 44, 659-665 (2009).
24. Hutchison, C. J. The role of DNA damage in laminopathy progeroid syndromes. Biochem. Soc. Trans. 39, 1715-1718 (2011).
25. Warren, D. T. & Shanahan, C. M. Defective DNA-damage repair induced by nuclear lamina dysfunction is a key mediator of smooth muscle cell aging. Biochem. Soc. Trans. 39, 1780-1785 (2011).
26. Shanahan, C M. Inflammation ushers in calcification: A cycle of damage and protection? Circulation 116, 2782-2785 (2007).
27. Iyemere, V. P. et al. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J. Intern. Med. 260, 192-210 (2006).
28. Shanahan, C. M. et al. Arterial calcification in chronic kidney disease: Key roles for calcium and phosphate. Circ. Res. 109, 697-711 (2011).
29. Jahnen-Dechent, W. et al. Fetuin A regulation of calcified matrix metabolism. Circ. Res. 108, 1494-1509 (2011).
30. McCabe, K. M. et al. Dietary vitamin K and therapeutic warfarin alter the susceptibility to vascular calcification in experimental chronic kidney disease. Kidney Int. 83, 835-844 (2013).
31. Yamada, S. et al. The antioxidant tempol ameliorates arterial medial calcification in uremic rats: Important role of oxidative stress in the pathogenesis of vascular calcification in chronic kidney disease. J. Bone Miner. Res. 27, 474-485 (2012).
32. Vaziri, N. D. Oxidative stress in uremia: Nature, mechanisms, and potential consequences. Semin. Nephrol. 24, 469-473 (2004).
33. Zhao, M. M. et al. Mitochondrial reactive oxygen species promote p65 nuclear translocation mediating high phosphate induced vascular calcification in vitro and in vivo. Kidney Int. 79, 1071-1079 (2011).
34. Shroff, R. C. et al. Dialysis accelerates medial vascular calcification in part by triggering smooth muscle cell apoptosis. Circulation 118, 1748-1757 (2008).
35. Reynolds, J. L. et al. 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. 15, 2857-2867 (2004).
36. Kapustin, A. N. et al. Calcium regulates key components of vascular smooth muscle cell-derived matrix vesicles to enhance mineralization. Circ. Res. 109, e1-e12 (2011).
37. Schlieper, G. et al. Ultrastructural analysis of vascular calcifications in uremia. J. Am. Soc. Nephrol. 21, 689-696 (2010).
38. Kapustin, A. N. & Shanahan, C. M. Calcium regulation of vascular smooth muscle cell-derived matrix vesicles. Trends Cardiovasc. Med. 22, 133-137 (2012).
39. Reynolds, J. L. et al. Multifunctional roles for serum protein fetuin a in inhibition of human vascular smooth muscle cell calcification. J. Am. Soc. Nephrol. 16, 2920-2930 (2005).
40. Ewence, A. E. et al. Calcium phosphate crystals induce cell death in human vascular smooth muscle cells: A potential mechanism in atherosclerotic plaque destabilization. Circ. Res. 103, e28-e34 (2008).
41. Sage, A. P. et al. Hyperphosphatemia-induced nanocrystals upregulate the expression of bone morphogenetic protein 2 and osteopontin genes in mouse smooth muscle cells in vitro. Kidney Int. 79, 414-422 (2011).
42. Bellasi, A. & Raggi, P. Vascular imaging in chronic kidney disease. Curr. Opin. Nephrol. Hypertens. 21, 382-388 (2012).
43. Speer, M. Y. et al. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ. Res. 104, 733-741 (2009).
44. Luo, G. et al. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386, 78-81 (1997).
45. Yao, Y. et al. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ. Res. 107, 485-494 (2010).
46. Westenfeld, R. et al. Effect of vitamin K2 supplementation on functional vitamin K deficiency in hemodialysis patients: A randomized trial. Am. J. Kidney Dis. 59, 186-195 (2012).
47. Hermans, M. M. et al. Association of serum fetuin A levels with mortality in dialysis patients. Kidney Int. 72, 202-207 (2007).
48. Fusaro, M. et al. Vitamin K, vertebral fractures, vascular calcifications, and mortality: VItamin K Italian (VIKI) dialysis study. J. Bone Miner. Res. 27, 2271-2278 (2012).
49. Fish, R. S. et al. ATP and arterial calcification. Eur. J. Clin. Invest. 43, 405-412 (2013).
50. Rutsch, F. et al. Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat. Genet. 34, 379-381 (2003).
51. Lomashvili, K. A. et al. Upregulation of alkaline phosphatase and pyrophosphate hydrolysis: Potential mechanism for uremic vascular calcification. Kidney Int. 73, 1024-1030 (2008).
52. Narisawa, S. et al. Novel inhibitors of alkaline phosphatase suppress vascular smooth muscle cell calcification. J. Bone Miner. Res. 22, 1700-1710 (2007).
53. O'Neill, W. C. Pyrophosphate, alkaline phosphatase, and vascular calcification. Circ. Res. 99, e2 (2006).
54. Lencel, P. et al. Cell-specific effects of TNF-alpha and IL 1beta on alkaline phosphatase: Implication for syndesmophyte formation and vascular calcification. Lab. Invest. 91, 1434-1442 (2011).
55. Ding, J. et al. TNF-alpha and IL 1beta inhibit RUNX2 and collagen expression but increase alkaline phosphatase activity and mineralization in human mesenchymal stem cells. Life Sci. 84, 499-504 (2009).
56. Zebboudj, A. F., Shin, V. & Bostrom, K. Matrix GLA protein and BMP 2 regulate osteoinduction in calcifying vascular cells. J. Cell. Biochem. 90, 756-765 (2003).
57. Schinke, T. et al. The serum protein alpha2-HS glycoprotein/fetuin inhibits apatite formation in vitro and in mineralizing calvaria cells. A possible role in mineralization and calcium homeostasis. J. Biol. Chem. 271, 20789-20796 (1996).
58. Schafer, C. et al. The serum protein alpha 2 Heremans Schmid glycoprotein/fetuin A is a systemically acting inhibitor of ectopic calcification. J. Clin. Invest. 112, 357-366 (2003).
59. Westenfeld, R. et al. Fetuin A protects against atherosclerotic calcification in CKD. J. Am. Soc. Nephrol. 20, 1264-1274 (2009).
60. Ketteler, M. et al. Association of low fetuin A (AHSG) concentrations in serum with cardiovascular mortality in patients on dialysis: A cross-sectional study. Lancet 361, 827-833 (2003).
61. Smith, E. R. et al. Serum fetuin A concentration and fetuin A containing calciprotein particles in patients with chronic inflammatory disease and renal failure. Nephrology (Carlton) 18, 215-221 (2013).
62. Smith, E. R. et al. Phosphorylated fetuin A containing calciprotein particles are associated with aortic stiffness and a procalcific milieu in patients with pre-dialysis CKD. Nephrol. Dial. Transplant. 27, 1957-1966 (2012).
63. Hamano, T. et al. Fetuin-mineral complex reflects extraosseous calcification stress in CKD. J. Am. Soc. Nephrol. 21, 1998-2007 (2010).
64. Pasch, A. et al. Nanoparticle-based test measures overall propensity for calcification in serum. J. Am. Soc. Nephrol. 23, 1744-1752 (2012).
65. Kuro-o, M. Klotho, phosphate and FGF 23 in ageing and disturbed mineral metabolism. Nat. Rev. Nephrol. http://dx.doi.org/10.1038/nrneph.2013.111.
66. Louvet, L. et al. Magnesium prevents phosphate-induced calcification in human aortic vascular smooth muscle cells. Nephrol. Dial. Transplant. 28, 869-878 (2013).
67. Schoppet, M et al. Exploring the biology of vascular calcification in chronic kidney disease: What's circulating? Kidney Int. 73, 384-390 (2008).
68. Salem, S. et al. Relationship between magnesium and clinical biomarkers on inhibition of vascular calcification. Am. J. Nephrol. 35, 31-39 (2012).
69. Tyson, K. L. et al. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler. Thromb. Vasc. Biol. 23, 489-494 (2003).
70. Tintut, Y. et al. Multilineage potential of cells from the artery wall. Circulation 108, 2505-2510 (2003).
71. Bostrom, K. I., Rajamannan, N. M. & Towler, D. A. The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ. Res. 109, 564-577 (2011).
72. Liu, Y. & Shanahan, C. M. Signalling pathways and vascular calcification. Front. Biosci. 16, 1302-1314 (2011).
73. Byon, C. H. et al. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J. Biol. Chem. 283, 15319-15327 (2008).
74. Li, X. & Giachelli, C. M. Sodium-dependent phosphate cotransporters and vascular calcification. Curr. Opin. Nephrol. Hypertens. 16, 325-328 (2007).
75. Voelkl, J. et al. Spironolactone ameliorates PIT1-dependent vascular osteoinduction in klotho-hypomorphic mice. J. Clin. Invest. 123, 812-822 (2013).
76. Cheng, S. L. et al. Activation of vascular smooth muscle parathyroid hormone receptor inhibits Wnt/beta-catenin signaling and aortic fibrosis in diabetic arteriosclerosis. Circ. Res. 107, 271-282 (2010).
77. Sun, Y. et al. Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification. Circ. Res. 111, 543-552 (2012).
78. Naik, V. et al. Sources of cells that contribute to atherosclerotic intimal calcification: An in vivo genetic fate mapping study. Cardiovasc. Res. 94, 545-554 (2012).
79. Lai, C. F. et al. TNFR1-activated reactive oxidative species signals up-regulate osteogenic Msx2 programs in aortic myofibroblasts. Endocrinology 153, 3897-3910 (2012).
80. Shroff, R. C. et al. Chronic mineral dysregulation promotes vascular smooth muscle cell adaptation and extracellular matrix calcification. J. Am. Soc. Nephrol. 21, 103-112 (2010).
81. Ohyama, Y. et al. Molecular cloning of rat klotho cDNA: Markedly decreased expression of klotho by acute inflammatory stress. Biochem. Biophys. Res. Commun. 251, 920-925 (1998).
82. Shimada, T. et al. Targeted ablation of Fgf23 demonstrates an essential physiological role of FGF23 in phosphate and vitamin D metabolism. J. Clin. Invest. 113, 561-568 (2004).
83. John, G. B., Cheng, C. Y. & Kuroo, M. Role of Klotho in aging, phosphate metabolism, and CKD. Am. J. Kidney Dis. 58, 127-134 (2011).
84. Moe, S. M. Klotho: A master regulator of cardiovascular disease? Circulation 125, 2181-2183 (2012).
85. Hu, M. C. et al. Klotho deficiency causes vascular calcification in chronic kidney disease. J. Am. Soc. Nephrol. 22, 124-136 (2011).
86. Kuroo, M. Klotho as a regulator of oxidative stress and senescence. Biol. Chem. 389, 233-241 (2008).
87. Liu, F. et al. Klotho suppresses RIG I mediated senescence-associated inflammation. Nat. Cell Biol. 13, 254-262 (2011).
88. Shiloh, Y. & Ziv, Y. The ATM protein kinase: Regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 14, 197-210 (2013).
89. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (2003).
90. Toussaint, O. et al. Stress-induced premature senescence and tissue ageing. Biochem. Pharmacol. 64, 1007-1009 (2002).
91. Rodier, F. et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol. 11, 973-979 (2009).
92. Song, Y. et al. Aging enhances the basal production of IL 6 and CCL2 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 32, 103-109 (2012).
93. Fyhrquist, F., Saijonmaa, O. & Strandberg, T. The roles of senescence and telomere shortening in cardiovascular disease. Nat. Rev. Cardiol. 10, 274-283 (2013).
94. Wang, J. C. & Bennett, M. Aging and atherosclerosis: Mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ. Res. 111, 245-259 (2012).
95. Jacobi, C., Hömme, M. & Melk, A. Is cellular senescence important in pediatric kidney disease? Pediatr. Nephrol. 26, 2121-2131 (2011).
96. Boxall, M. C. et al. Telomere shortening and haemodialysis. Blood Purif. 24, 185-189 (2006).
97. Stenvinkel, P. & Larsson, T. E. Chronic kidney disease: A clinical model of premature aging. Am. J. Kidney Dis. 62, 339-351 (2013).
98. Ragnauth, C. D. et al. Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation 121, 2200-2210 (2010).
99. Gerhard-Herman, M. et al. Mechanisms of premature vascular aging in children with Hutchinson-Gilford progeria syndrome. Hypertension 59, 92-97 (2012).
100. Mounkes, L. C. & Stewart, C. L. Aging and nuclear organization: Lamins and progeria. Curr. Opin. Cell Biol. 16, 322-327 (2004).
101. McClintock, D., Gordon, L. B. & Djabali, K. Hutchinson-Gilford progeria mutant lamin A primarily targets human vascular cells as detected by an anti-Lamin A G608G antibody. Proc. Natl Acad. Sci. USA 103, 2154-2159 (2006).
102. Richards, S. A. et al. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N acetyl cysteine. Hum. Mol. Genet. 20, 3997-4004 (2011).
103. Muteliefu, G. et al. Indoxyl sulfate promotes vascular smooth muscle cell senescence with upregulation of p53, p21, and prelamin A through oxidative stress. Am. J. Physiol. Cell Physiol. 303, C126-C134 (2012).
104. Liu, B. et al. Genomic instability in laminopathy-based premature aging. Nat. Med. 11, 780-785 (2005).
105. Ugalde, A. P. et al. Aging and chronic DNA damage response activate a regulatory pathway involving miR 29 and p53. EMBO J. 30, 2219-2232 (2011).
106. Gordon, L. B. et al. Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 109, 16666-16671 (2012).
107. Varela, I. et al. Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat. Med. 14, 767-772 (2008).
108. Liu, Y. et al. DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A.J. Cell Sci. 119, 4644-4649 (2006).
109. Chaki, M. et al. Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling. Cell 150, 533-548 (2012).
110. Zhou, W. et al. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 44, 910-915 (2012).
111. Rasheed, N. et al. Atm-deficient mice: An osteoporosis model with defective osteoblast differentiation and increased osteoclastogenesis. Hum. Mol. Genet. 15, 1938-1948 (2006).
112. Durik, M. et al. Nucleotide excision DNA repair is associated with age-related vascular dysfunction. Circulation 126, 468-478 (2012).
113. Zhang, J. et al. A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8, 31-45 (2011).
114. Scaffidi, P. & Misteli, T. Lamin A dependent misregulation of adult stem cells associated with accelerated ageing. Nat. Cell Biol. 10, 452-459 (2008).
115. Agarwal, A. K. et al. Focal segmental glomerulosclerosis in patients with mandibuloacral dysplasia owing to ZMPSTE24 deficiency. J. Investig. Med. 54, 208-213 (2006).
116. Imachi, H. et al. A case of Dunnigan-type familial partial lipodystrophy (FPLD) due to lamin A/C (LMNA) mutations complicated by end-stage renal disease. Endocrine 35, 18-21 (2009).
117. Ahmad, Z. et al. Early onset mandibuloacral dysplasia due to compound heterozygous mutations in ZMPSTE24. Am. J. Med. Genet. A 152A, 2703-2710 (2010).
118. Osorio, F. G. et al. Nuclear lamina defects cause ATM-dependent NF kappaB activation and link accelerated aging to a systemic inflammatory response. Genes Dev. 26, 2311-2324 (2012).
119. Dalfino, G. et al. Bone morphogenetic protein 2 may represent the molecular link between oxidative stress and vascular stiffness in chronic kidney disease. Atherosclerosis 211, 418-423 (2010).
120. Wei, J. et al. Increase of plasma IL 6 concentration with age in healthy subjects. Life Sci. 51, 1953-1956 (1992).
121. Nitta, K. et al. Serum osteoprotegerin levels and the extent of vascular calcification in haemodialysis patients. Nephrol. Dial. Transplant. 19, 1886-1889 (2004).
122. Takemura, A. et al. Sirtuin 1 retards hyperphosphatemia-induced calcification of vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 31, 2054-2062 (2011).
123. Tang, Y. et al. Resveratrol reduces vascular cell senescence through attenuation of oxidative stress by SIRT1/NADPH oxidase-dependent mechanisms. J. Nutr. Biochem. 23, 1410-1416 (2012).