Phosphate-induced autophagy counteracts vascular calcification by reducing matrix vesicle release

Kidney International

Volumn 83, Issue 6, 2013, Pages 1042-1051

  Dai, Xiao Yan ^a   Zhao, Ming Ming ^a   Cai, Yan ^a   Guan, Qing Cong ^b   Zhao, Ying ^a   Guan, Youfei ^a   Kong, Wei ^a   Zhu, Wei Guo ^a   Xu, Ming Jiang ^a   Wang, Xian ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Renal Division   (China)

Author keywords

Apoptosis; Autophagy; Chronic renal failure; Hyperphosphatemia; Oxidative stress

Indexed keywords

3 METHYLADENINE; ALKALINE PHOSPHATASE; APOPTOSIS INHIBITOR; AUTOPHAGY PROTEIN 5; CALCIUM; CASPASE 3; CASPASE 7; LIPOCORTIN 2; MANGANESE SUPEROXIDE DISMUTASE; PHOSPHATE; PORPHYRIN DERIVATIVE; REACTIVE OXYGEN METABOLITE; SODIUM PHOSPHATE COTRANSPORTER; TRANSCRIPTION FACTOR PIT 1;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BLOOD VESSEL CALCIFICATION; CELL SURVIVAL; CELL VACUOLE; CHRONIC KIDNEY FAILURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; KIDNEY TRANSPLANTATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; UREMIA; VASCULAR SMOOTH MUSCLE;

EID: 84882264646     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2012.482     Document Type: Article

References (47)

1. Meijer AJ. Amino acids as regulators and components of nonproteinogenic pathways. J Nutr 2003; 133: 2057S-2062S.
2. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
3. Cuervo AM. Autophagy: in sickness and in health. Trends Cell Biol 2004; 14: 70-77.
4. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004; 306: 990-995.
5. De Meyer GR, Martinet W. Autophagy in the cardiovascular system. Biochim Biophys Acta 2009; 1793: 1485-1495.
6. Martinet W, De Meyer GR. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res 2009; 104: 304-317.
7. Zhang H, Bosch-Marce M, Shimoda LA et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 2008; 283: 10892-10903.
8. Crighton D, Wilkinson S, O'Prey J et al. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 2006; 126: 121-134.
9. London GM, Guerin AP, Marchais SJ et al. Arterial media calcification in end-stage renal disease: impact on all-cause and cardiovascular mortality. Nephrol Dial Transplant 2003; 18: 1731-1740.
10. Block GA, Port FK. Re-evaluation of risks associated with hyperphosphatemia and hyperparathyroidism in dialysis patients: recommendations for a change in management. Am J Kidney Dis 2000; 35: 1226-1237.
11. Giachelli CM, Jono S, Shioi A et al. Vascular calcification and inorganic phosphate. Am J Kidney Dis 2001; 38: S34-S37.
12. Ohnishi M, Nakatani T, Lanske B et al. In vivo genetic evidence for suppressing vascular and soft-tissue calcification through the reduction of serum phosphate levels, even in the presence of high serum calcium and 1,25-dihydroxyvitamin D levels. Circ Cardiovasc Genet 2009; 2: 583-590.
13. Giachelli CM. The emerging role of phosphate in vascular calcification. Kidney Int 2009; 75: 890-897.
14. Shanahan CM, Crouthamel MH, Kapustin A et al. Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ Res 109: 697-711.
15. Zhao MM, Xu MJ, Cai Y 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.
16. Zhao G, Xu MJ, Zhao MM et al. Activation of nuclear factor-kappa B accelerates vascular calcification by inhibiting ankylosis protein homolog expression. Kidney Int 82: 34-44.
17. Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16: 1040-1052.
18. Chen Y, Gibson SB. Is mitochondrial generation of reactive oxygen species a trigger for autophagy? Autophagy 2008; 4: 246-248.
19. Huang J, Lam GY, Brumell JH. Autophagy signaling through reactive oxygen species. Antioxid Redox Signal 14: 2215-2231.
20. Srinivas V, Bohensky J, Zahm AM et al. Autophagy in mineralizing tissues: microenvironmental perspectives. Cell Cycle 2009; 8: 391-393.
21. Son BK, Kozaki K, Iijima K et al. Statins protect human aortic smooth muscle cells from inorganic phosphate-induced calcification by restoring Gas6-Axl survival pathway. Circ Res 2006; 98: 1024-1031.
22. Proudfoot D, Skepper JN, Hegyi L et al. Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ Res 2000; 87: 1055-1062.
23. Mizushima N, Levine B, Cuervo AM et al. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-1075.
24. Li X, Yang HY, Giachelli CM. Role of the sodium-dependent phosphate cotransporter, Pit-1, in vascular smooth muscle cell calcification. Circ Res 2006; 98: 905-912.
25. Kiffin R, Bandyopadhyay U, Cuervo AM. Oxidative stress and autophagy. Antioxid Redox Signal 2006; 8: 152-162.
26. Maiuri MC, Zalckvar E, Kimchi A et al. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8: 741-752.
27. Scott RC, Juhasz G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol 2007; 17: 1-11.
28. Espert L, Denizot M, Grimaldi M et al. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J Clin Invest 2006; 116: 2161-2172.
29. Yousefi S, Perozzo R, Schmid I et al. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol 2006; 8: 1124-1132.
30. Anderson HC. Matrix vesicles and calcification. Curr Rheumatol Rep 2003; 5: 222-226.
31. Reynolds JL, Joannides AJ, Skepper JN 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 2004; 15: 2857-2867.
32. Chen NX, O'Neill KD, Chen X et al. Annexin-mediated matrix vesicle calcification in vascular smooth muscle cells. J Bone Miner Res 2008; 23: 1798-1805.
33. Woeckel VJ, Alves RD, Swagemakers SM et al. 1Alpha,25-(OH)2D3 acts in the early phase of osteoblast differentiation to enhance mineralization via accelerated production of mature matrix vesicles. J Cell Physiol 225: 593-600.
34. Chen NX, Kircelli F, O'Neill KD et al. Verapamil inhibits calcification and matrix vesicle activity of bovine vascular smooth muscle cells. Kidney Int 77: 436-442.
35. Dean DD, Schwartz Z, Bonewald L et al. Matrix vesicles produced by osteoblast-like cells in culture become significantly enriched in proteoglycan-degrading metalloproteinases after addition of betaglycerophosphate and ascorbic acid. Calcif Tissue Int 1994; 54: 399-408.
36. Hale JE, Wuthier RE. The mechanism of matrix vesicle formation. Studies on the composition of chondrocyte microvilli and on the effects of microfilament-perturbing agents on cellular vesiculation. J Biol Chem 1987; 262: 1916-1925.
37. Hale JE, Chin JE, Ishikawa Y et al. Correlation between distribution of cytoskeletal proteins and release of alkaline phosphatase-rich vesicles by epiphyseal chondrocytes in primary culture. Cell Motil 1983; 3: 501-512.
38. Thouverey C, Strzelecka-Kiliszek A, Balcerzak M et al. Matrix vesicles originate from apical membrane microvilli of mineralizing osteoblast-like Saos-2 cells. J Cell Biochem 2009; 106: 127-138.
39. Mostowy S, Cossart P. Autophagy and the cytoskeleton: new links revealed by intracellular pathogens. Autophagy 7: 780-782.
40. Riediger F, Quack I, Qadri F et al. Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 22: 2193-2202.
41. Frye MA, Melton LJ III, Bryant SC et al. Osteoporosis and calcification of the aorta. Bone Miner 1992; 19: 185-194.
42. Kiel DP, Kauppila LI, Cupples LA et al. Bone loss and the progression of abdominal aortic calcification over a 25 year period: the Framingham Heart Study. Calcif Tissue Int 2001; 68: 271-276.
43. Rodriguez Garcia M, Naves Diaz M, Cannata Andia JB. Bone metabolism, vascular calcifications and mortality: associations beyond mere coincidence. J Nephrol 2005; 18: 458-463.
44. Ross R. The smooth muscle cell. II. Growth of smooth muscle in culture and formation of elastic fibers. J Cell Biol 1971; 50: 172-186.
45. Shioi A, Nishizawa Y, Jono S et al. Beta-glycerophosphate accelerates calcification in cultured bovine vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1995; 15: 2003-2009.
46. Cai Y, Xu MJ, Teng X et al. Intermedin inhibits vascular calcification by increasing the level of matrix gamma-carboxyglutamic acid protein. Cardiovasc Res 85: 864-873.
47. Wuthier RE, Chin JE, Hale JE et al. Isolation and characterization of calcium-accumulating matrix vesicles from chondrocytes of chicken epiphyseal growth plate cartilage in primary culture. J Biol Chem 1985; 260: 15972-15979.