Dialysis accelerates medial vascular calcification in part by triggering smooth muscle cell apoptosis

Circulation

Volumn 118, Issue 17, 2008, Pages 1748-1757

  Shroff, Rukshana C ^a,b   McNair, Rosamund ^c   Figg, Nichola ^c   Skepper, Jeremy N ^d   Schurgers, Leon ^e   Gupta, Ashmeet ^a   Hiorns, Melanie ^a   Donald, Ann E ^a   Deanfield, John ^a   Rees, Lesley ^a   Shanahan, Catherine M ^b,f  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d Multi Imaging Centre   (United Kingdom)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f BHF Centre

Author keywords

Apoptosis; Calcification, vascular; Cardiovascular disease; Kidney diseases; Muscles, vascular smooth; Pediatrics; Vesicles, vascular smooth muscle cell derived

Indexed keywords

ALKALINE PHOSPHATASE; CALCIUM; CALPHOBINDIN II; FETUIN A; OSTEOCALCIN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2;

APOPTOSIS; ARTERIAL STIFFNESS; ARTERIAL WALL THICKNESS; ARTICLE; BLOOD VESSEL CALCIFICATION; BLOOD VESSEL INJURY; CARDIOVASCULAR RISK; CELL TRANSFORMATION; CLINICAL ARTICLE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIALYSIS; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; OSTEOBLAST; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; BLOOD; CALCINOSIS; CHILD; COMPARATIVE STUDY; MESENTERIC ARTERY; METABOLISM; PATHOLOGY; PHYSIOLOGY; RENAL REPLACEMENT THERAPY; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE;

APOPTOSIS; CALCINOSIS; CALCIUM; CHILD; HUMANS; MESENTERIC ARTERIES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RENAL DIALYSIS; VASCULAR DISEASES;

EID: 55449101447     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.783738     Document Type: Article

References (42)

1. Foley RN, Parfrey PS, Sarnak MJ. Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis. 1998;32:S112-S119.
2. Groothoff JW, Gruppen MP, Offringa M, Hutten J, Lilien MR, Van De Kar NJ, Wolff ED, Davin JC, Heymans HS. Mortality and causes of death of end-stage renal disease in children: a Dutch cohort study. Kidney Int. 2002;61:621-629.
3. Kari JA, Donald AE, Vallance DT, Bruckdorfer KR, Leone A, Mullen MJ, Bunce T, Dorado B, Deanfield JE, Rees L. Physiology and biochemistry of endothelial function in children wich chronic renal failure. Kidney Int. 1997;52:468-472.
4. Shroff RC, Donald AE, Hiorns MP, Watson A, Feather S, Milford D, Ellins EA, Stony C, Ridout D, Deanfield J, Rees L. Mineral metabolism and vascular damage in children on dialysis. J Am Soc Nephrol. 2007;18:2996-3003.
5. Shroff R, Egerton M, Bridel M, Shah V, Donald A, Cole T, Hiorns M, Deanfield J, and Rees L. Vitamin D has a bimodal effect on vascular structure and calcification in children on dialysis via its calciotropic and anti-inflammatory effects. J Am Soc Nephrol. 2008;19:1239-1246.
6. Goldsmith D, Ritz E, Covic A. Vascular calcification: a stiff challenge for the nephrologist: does preventing bone disease cause arterial disease? Kidney Int. 2004;66:1315-1333.
7. Block GA, Hulbert-Shearon TE, Levin NW, Port FK. 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.
8. Litwin M, Wuhl E, Jourdan C, Trelewicz J, Niemirska A, Fahr K, Jobs K, Grenda R, Wawer ZT, Rajszys P, Troger J, Mehls O, Schaefer F. Altered morphologic properties of large arteries in children with chronic renal failure and after renal transplantation. J Am Soc Nephrol. 2005;16:1494-1500.
9. Mitsnefes MM, Kimball TR, Witt SA, Glascock BJ, Khoury PR, Daniels SR. Abnormal carotid artery structure and function in children and adolescents with successful renal transplantation. Circulation. 2004;110:97-101.
10. Oh J, Wunsch R, Turzer M, Bahner M, Raggi P, Querfeld U, Mehls O, Schaefer F. Advanced coronary and carotid arteriopathy in young adults with childhood-onset chronic renal failure. Circulation. 2002;106:100-105.
11. Covic A, Mardare N, Gusbeth-Tatomir P, Brumaru O, Gavrilovici C, Munteanu M, Prisada O, Goldsmith DJ. Increased arterial stiffness in children on haemodialysis. Nephrol Dial Transplant. 2006;21:729-735.
12. Goodman WG, Goldin J, Kuizon BD, Yoon C, Gales B, Sider D, Wang Y, Chung J, Emerick A, Greaser L, Elashoff RM, Salusky IB. Coronary-artery calcification in young adults with end-stage renal disease who are undergoing dialysis. N Engl J Med. 2000;342:1478-1483.
13. Milliner DS, Zinsmeister AR, Lieberman E. Landing B. Soft tissue calcification in pediatric patients with end-stage renal disease. Kidney Int. 1990;38:931-936.
14. Shanahan CM, Cary NR, Salisbury JR, Proudfoot D, Weissberg PL, Edmonds ME. Medial localization of mineralization-regulating proteins in association widi Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation. 1999;100:2168-2176.
15. Tyson KL, Reynolds JL, McNair R, Zhang Q. Weissberg PL, Shanahan CM. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol. 2003;23:489-494.
16. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, Weissberg PL. Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ Res. 2000;87:1055-1062.
17. Reynolds JL, Joannides AJ, Skepper JN, McNair R, Schurgers LJ, Proudfoot D, Jahnen-Dechent W, Weissberg PL, Shanahan CM. 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.
18. Reynolds JL, Skepper JN, McNair R, Kasama T, Gupta K, Weissberg PL, Jahnen-Dechent W, Shanahan CM. Multifunctional roles for serum protein fetuin-a in inhibition of human vascular smooth muscle cell calcification. J Am Soc Nephrol. 2005;16:2920-2930.
19. Proudfoot D, Shanahan CM. Molecular mechanisms mediating vascular calcification: role of matrix Gla protein. Nephrology (Carlton). 2006;11: 455-461.
20. Shanahan CM, Proudfoot D, Farzaneh-Far A, Weissberg PL. The role of GIa proteins in vascular calcification. Crit Rev Eukaryot Gene Expr. 1998;8:357-375.
21. Moe SM, O'Neill KD, Duan D, Ahmed S, Chen NX, Leapman SB, Fineberg N, Kopecky K. Medial artery calcification in ESRD patients is associated with deposition of bone matrix proteins. Kidney Int. 2002;61:638-647.
22. Moe SM, Duan D, Doehle BP, O'Neill KD, Chen NX. Uremia induces me osteoblast differentiation factor Cbfa1 in human blood vessels. Kidney Int. 2003;63:1003-1011.
23. Ketteler M, Bongartz P, Westenfeld R, Wildberger JE, Mahnken AH, Bohm R, Metzger T, Wanner C, Jahnen-Dechent W, Floege J. Association of low fetuin-A (AHSG) concentrations in serum with cardiovascular mortality in patients on dialysis: a cross-sectional study. Lancet. 2003;361:827-833.
24. Schurgers LJ, Spronk HM, Skepper JN, Hackeng TM, Shanahan CM, Vermeer C, Weissberg PL, Proudfoot D. Post-translational modifications regulate matrix Gla protein function: importance for inhibition of vascular smooth muscle cell calcification. J Thromb Haemost. 2007;5:2503-2511.
25. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR, Karsenty G. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature. 1997;386:78-81.
26. Westenfeld R, Schafer C, Smeets R, Brandenburg VM, Floege J, Ketteler M, Jahnen-Dechent W. Fetuin-A (AHSG) prevents extraosseous calcification induced by uraemia and phosphate challenge in mice. Nephrol Dial Transplant. 2007;22:1537-1546.
27. Block GA, Spiegel DM, Ehrlich J, Mehta R, Lindbergh J, Dreisbach A, Raggi P. Effects of sevelamer and calcium on coronary artery calcification in patients new to hemodialysis. Kidney Int. 2005;68:1815-1824.
28. Toussaint ND, Lau KK, Strauss BJ, Polkinghorne KR, Kerr PG. Associations between vascular calcification, arterial stiffness and bone mineral density in chronic kidney disease. Nephrol Dial Transplant. 2007;23:586-593.
29. Olszak IT, Poznansky MC, Evans RH, Olson D, Kos C, Pollak MR, Brown EM, Scadden DT. Extracellular calcium elicits a chemokinetic response from monocytes in vitro and in vivo. J Clin Invest. 2000;105:1299-1305.
30. Soriano S, Gonzalez L, Martin-Malo A, Rodriguez M, Aljama P. C-reactive protein and low albumin are predictors of morbidity and cardiovascular events in chronic kidney disease (CKD) 3-5 patients. Clin Nephrol. 2007;67:352-357.
31. Shanahan CM. Vascular calcification: a matter of damage limitation? Nephrol Dial Transplant. 2006;21:1166-1169.
32. Ishimura E, Okuno S, Kitatani K, Kim M, Shoji T, Nakatani T, Inaba M, Nishizawa Y. Different risk factors for peripheral vascular calcification between diabetic and non-diabetic haemodialysis patients: importance of glycaemic control. Diabetologia. 2002;45:1446-1448.
33. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, rley-Usmar VM, McDonald JM, Chen Y. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem. 2008;283:15319-15327.
34. Rogers NM, Teubner DJ, Coates PT. Calcific uremic arteriolopathy: advances in pathogenesis and treatment. Semin Dial. 2007;20:150-157.
35. Schurgers LJ, Teunissen KJ, Knapen MH, Kwaijtaal M, van DR, Appels A, Reutelingsperger CP, Cleutjens JP, Vermeer C. Novel conformation-specific antibodies against matrix gamma-carboxyglutamic acid (Gla) protein: undercarboxylated matrix Gla protein as marker for vascular calcification. Arterioscler Thromb Vasc Biol. 2005;25:1629-1633.
36. Walsh K, Shiojima I, Gualberto A. DNA replication and smooth muscle cell hypertrophy. J Clin Invest. 1999;104:673-674.
37. Lomashvili KA, Cobbs S, Hennigar RA, Hardcastle KI, O'Neill WC. Phosphate-induced vascular calcification: role of pyrophosphate and osteopontin. J Am Soc Nephrol. 2004;15:1392-1401.
38. Rutsch F, Ruf N, Vaingankar S, Toliat MR, Suk A, Hohne W, Schauer G, Lehmann M, Roscioli T, Schnabel D, Epplen JT, Knisely A, Superti-Furga A, McGill J, Filippone M, Sinaiko AR, Vallance H, Hinrichs B, Smith W, Ferre M, Terkeltaub R, Nurnberg P. Mutations in ENPP1 are associated with "idiopathic" infantile arterial calcification. Nat Genet. 2003;34:379-381.
39. Minguell JJ, Fierro FA, Epunan MJ, Erices AA, Sierralta WD. Non-stimulated human uncommitted mesenchymal stem cells express cell markers of mesenchymal and neural lineages. Stem Cells Dev. 2005;14:408-414.
40. Liberman M, Bassi E, Martinatti MK, Lario FC, Wosniak J Jr, Pomerantzeff PM, Laurindo FR. Oxidant generation predominates around calcifying foci and enhances progression of aortic valve calcification. Arterioscler Thromb Vasc Biol. 2008;28:463-470.
41. Harrington KS, Javed A, Drissi H, McNeil S, Lian JB, Stein JL, Van Wijnen AJ, Wang YL, Stein GS. Transcription factors RUNX1/AML1 and RUNX2/Cbfal dynamically associate with stationary subnuclear domains. J Cell Sci. 2002;115:4167-4176.
42. Terry A, Kilbey A, Vaillant F, Stewart M, Jenkins A, Cameron E, Neil JC. Conservation and expression of an alternative 3′ exon of Runx2 encoding a novel proline-rich C-terminal domain. Gene. 2004;336:115-125.