Hypoxia-inducible factor-1 plays a role in phosphate-induced vascular smooth muscle cell calcification

Kidney International

Volumn 90, Issue 3, 2016, Pages 598-609

  Mokas, Sophie ^a   Larivière, Richard ^a   Lamalice, Laurent ^a   Gobeil, Stéphane ^a   Cornfield, David N ^b   Agharazii, Mohsen ^a   Richard, Darren E ^a  

^a LAVAL UNIVERSITY   (Canada)

^b STANFORD UNIVERSITY   (United States)

Author keywords

chronic kidney disease; HIF 1; hypoxia; mineral imbalance; vascular calcification

Indexed keywords

ANTIOXIDANT; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PHOSPHATE; SKQ 1; STIGMATELLIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; FG-4592; GLYCINE; HIF1A PROTEIN, RAT; ISOQUINOLINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL CALCIFICATION; CELL HYPOXIA; CELL TRANSDIFFERENTIATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; DRUG TARGETING; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; THORACIC AORTA; VASCULAR SMOOTH MUSCLE; ANALOGS AND DERIVATIVES; ANIMAL; ARTERIAL STIFFNESS; CELL CULTURE; CHRONIC KIDNEY FAILURE; COMPLICATION; CYTOLOGY; DISEASE MODEL; HUMAN; HYPOXIA; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; VASCULAR CALCIFICATION; WISTAR RAT;

ANIMALS; BIOMARKERS; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GLYCINE; HUMANS; HYPOXIA; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; ISOQUINOLINES; MALE; MUSCLE, SMOOTH, VASCULAR; PHOSPHATES; RATS; RATS, WISTAR; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION; VASCULAR CALCIFICATION; VASCULAR STIFFNESS;

EID: 84979700573     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2016.05.020     Document Type: Article

References (71)

1. 1 Mizobuchi, M., Towler, D., Slatopolsky, E., Vascular calcification: the killer of patients with chronic kidney disease. J Am Soc Nephrol 20 (2009), 1453–1464.
2. 2 Johnson, R.C., Leopold, J.A., Loscalzo, J., Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res 99 (2006), 1044–1059.
3. 3 Paloian, N.J., Giachelli, C.M., A current understanding of vascular calcification in CKD. Am J Physiol Renal Physiol 307 (2014), F891–F900.
4. 4 Kendrick, J., Chonchol, M., The role of phosphorus in the development and progression of vascular calcification. Am J Kidney Dis 58 (2011), 826–834.
5. 5 Lau, W.L., Pai, A., Moe, S.M., Giachelli, C.M., Direct effects of phosphate on vascular cell function. Adv Chronic Kidney Dis 18 (2011), 105–112.
6. 6 Ryoo, H.M., Lee, M.H., Kim, Y.J., Critical molecular switches involved in BMP-2-induced osteogenic differentiation of mesenchymal cells. Gene 366 (2006), 51–57.
7. 7 Li, X., Yang, H.Y., Giachelli, C.M., BMP-2 promotes phosphate uptake, phenotypic modulation, and calcification of human vascular smooth muscle cells. Atherosclerosis 199 (2008), 271–277.
8. 8 Yao, Y., Bennett, B.J., Wang, X., et al. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ Res 107 (2010), 485–494.
9. 9 Shroff, R., Long, D.A., Shanahan, C., Mechanistic insights into vascular calcification in CKD. J Am Soc Nephrol 24 (2013), 179–189.
10. 10 Bruderer, M., Richards, R.G., Alini, M., Stoddart, M.J., Role and regulation of RUNX2 in osteogenesis. Eur Cell Mater 28 (2014), 269–286.
11. 11 Steitz, S.A., Speer, M.Y., Curinga, G., et al. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res 89 (2001), 1147–1154.
12. 12 Tyson, K.L., Reynolds, J.L., McNair, R., et al. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol 23 (2003), 489–494.
13. 13 Cachofeiro, V., Goicochea, M., de Vinuesa, S.G., et al. Oxidative stress and inflammation, a link between chronic kidney disease and cardiovascular disease. Kidney Int Suppl(111), 2008, S4–S9.
14. 14 Chen, N.X., Moe, S.M., Vascular calcification: pathophysiology and risk factors. Curr Hypertens Rep 14 (2012), 228–237.
15. 15 Nangaku, M., Eckardt, K.U., Hypoxia and the HIF system in kidney disease. J Mol Med (Berl) 85 (2007), 1325–1330.
16. 16 Gunaratnam, L., Bonventre, J.V., HIF in kidney disease and development. J Am Soc Nephrol 20 (2009), 1877–1887.
17. 17 Araldi, E., Schipani, E., Hypoxia, HIFs and bone development. Bone 47 (2010), 190–196.
18. 18 Hirao, M., Hashimoto, J., Yamasaki, N., et al. Oxygen tension is an important mediator of the transformation of osteoblasts to osteocytes. J Bone Miner Metab 25 (2007), 266–276.
19. 19 Idelevich, A., Rais, Y., Monsonego-Ornan, E., Bone Gla protein increases HIF-1alpha-dependent glucose metabolism and induces cartilage and vascular calcification. Arterioscler Thromb Vasc Biol 31 (2011), e55–e71.
20. 20 Li, G., Lu, W.H., Ai, R., et al. The relationship between serum hypoxia-inducible factor 1α and coronary artery calcification in asymptomatic type 2 diabetic patients. Cardiovasc Diabetol, 13, 2014, 52.
21. 21 Michaud, M.D., Robitaille, G.A., Gratton, J.P., Richard, D.E., Sphingosine-1-phosphate: a novel nonhypoxic activator of hypoxia-inducible factor-1 in vascular cells. Arterioscler Thromb Vasc Biol 29 (2009), 902–908.
22. 22 Majmundar, A.J., Wong, W.J., Simon, M.C., Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40 (2010), 294–309.
23. 23 Jiang, B.H., Rue, E., Wang, G.L., et al. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 271 (1996), 17771–17778.
24. 24 Kaelin, W.G. Jr., Ratcliffe, P.J., Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30 (2008), 393–402.
25. 25 Bruick, R.K., McKnight, S.L., A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294 (2001), 1337–1340.
26. 26 Epstein, A.C., Gleadle, J.M., McNeill, L.A., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107 (2001), 43–54.
27. 27 Ivan, M., Kondo, K., Yang, H., et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292 (2001), 464–468.
28. 2-regulated prolyl hydroxylation. Science 292 (2001), 468–472.
29. 29 Maxwell, P.H., Wiesener, M.S., Chang, G.W., et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399 (1999), 271–275.
30. 30 Schofield, C.J., Ratcliffe, P.J., Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5 (2004), 343–354.
31. 31 Agharazii, M., St-Louis, R., Gautier-Bastien, A., et al. Inflammatory cytokines and reactive oxygen species as mediators of chronic kidney disease-related vascular calcification. Am J Hypertens 28 (2015), 746–755.
32. 32 Gauthier-Bastien, A., Ung, R.V., Lariviere, R., et al. Vascular remodeling and media calcification increases arterial stiffness in chronic kidney disease. Clin Exp Hypertens 36 (2014), 173–180.
33. 33 Jono, S., McKee, M.D., Murry, C.E., et al. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res 87 (2000), E10–E17.
34. 34 Carreau, A., El Hafny-Rahbi, B., Matejuk, A., et al. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med 15 (2011), 1239–1253.
35. 35 Patten, D.A., Lafleur, V.N., Robitaille, G.A., et al. Hypoxia-inducible factor-1 activation in nonhypoxic conditions: the essential role of mitochondrial-derived reactive oxygen species. Mol Biol Cell 21 (2010), 3247–3257.
36. 2 tension. Proc Natl Acad Sci U S A 92 (1995), 5510–5514.
37. 37 Besarab, A., Provenzano, R., Hertel, J., et al. Randomized placebo-controlled dose-ranging and pharmacodynamics study of roxadustat (FG-4592) to treat anemia in nondialysis-dependent chronic kidney disease (NDD-CKD) patients. Nephrol Dial Transplant 30 (2015), 1665–1673.
38. 38 Provenzano, R., Besarab, A., Wright, S., et al. Roxadustat (FG-4592) versus epoetin alfa for anemia in patients receiving maintenance hemodialysis: a phase 2, randomized, 6- to 19-week, open-label, active-comparator, dose-ranging, safety and exploratory efficacy study. Am J Kidney Dis 67 (2016), 912–924.
39. 39 Kim, Y.M., Barnes, E.A., Alvira, C.M., et al. Hypoxia-inducible factor-1α in pulmonary artery smooth muscle cells lowers vascular tone by decreasing myosin light chain phosphorylation. Circ Res 112 (2013), 1230–1233.
40. 40 Dery, M.A., Michaud, M.D., Richard, D.E., Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37 (2005), 535–540.
41. 41 Salnikow, K., Donald, S.P., Bruick, R.K., et al. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 279 (2004), 40337–40344.
42. 42 Page, E.L., Chan, D.A., Giaccia, A.J., et al. Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol Cell 19 (2008), 86–94.
43. 43 Abedin, M., Tintut, Y., Demer, L.L., Vascular calcification: mechanisms and clinical ramifications. Arterioscler Thromb Vasc Biol 24 (2004), 1161–1170.
44. 44 Semenza, G.L., Hypoxia-inducible factor 1 and cardiovascular disease. Annu Rev Physiol 76 (2014), 39–56.
45. 45 Maes, C., Carmeliet, G., Schipani, E., Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol 8 (2012), 358–366.
46. 46 O'Neill, W.C., Adams, A.L., Breast arterial calcification in chronic kidney disease: absence of smooth muscle apoptosis and osteogenic transdifferentiation. Kidney Int 85 (2014), 668–676.
47. 47 El-Abbadi, M.M., Pai, A.S., Leaf, E.M., et al. Phosphate feeding induces arterial medial calcification in uremic mice: role of serum phosphorus, fibroblast growth factor-23, and osteopontin. Kidney Int 75 (2009), 1297–1307.
48. 48 Ivandic, B.T., Utz, H.F., Kaczmarek, P.M., et al. New Dyscalc loci for myocardial cell necrosis and calcification (dystrophic cardiac calcinosis) in mice. Physiol Genomics 6 (2001), 137–144.
49. 49 Speer, M.Y., Li, X., Hiremath, P.G., Giachelli, C.M., Runx2/Cbfa1, but not loss of myocardin, is required for smooth muscle cell lineage reprogramming toward osteochondrogenesis. J Cell Biochem 110 (2010), 935–947.
50. 50 Sun, Y., Byon, C.H., Yuan, K., et al. Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification. Circ Res 111 (2012), 543–552.
51. 51 Kwon, T.G., Zhao, X., Yang, Q., et al. Physical and functional interactions between Runx2 and HIF-1α induce vascular endothelial growth factor gene expression. J Cell Biochem 112 (2011), 3582–3593.
52. 52 Lee, S.H., Che, X., Jeong, J.H., et al. Runx2 protein stabilizes hypoxia-inducible factor-1α through competition with von Hippel-Lindau protein (pVHL) and stimulates angiogenesis in growth plate hypertrophic chondrocytes. J Biol Chem 287 (2012), 14760–14771.
53. 53 Ferrara, N., Gerber, H.P., LeCouter, J., The biology of VEGF and its receptors. Nat Med 9 (2003), 669–676.
54. 54 Forsythe, J.A., Jiang, B.H., Iyer, N.V., et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16 (1996), 4604–4613.
55. 55 Deckers, M.M., Karperien, M., van der Bent, C., et al. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141 (2000), 1667–1674.
56. 56 Gerber, H.P., Vu, T.H., Ryan, A.M., et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5 (1999), 623–628.
57. 57 Zelzer, E., McLean, W., Ng, Y.S., et al. Skeletal defects in VEGF(120/120) mice reveal multiple roles for VEGF in skeletogenesis. Development 129 (2002), 1893–1904.
58. 58 Zelzer, E., Glotzer, D.J., Hartmann, C., et al. Tissue specific regulation of VEGF expression during bone development requires Cbfa1/Runx2. Mech Dev 106 (2001), 97–106.
59. 59 Liu, Y., Berendsen, A.D., Jia, S., et al. Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J Clin Invest 122 (2012), 3101–3113.
60. 60 Rumsey, S.C., Kwon, O., Xu, G.W., et al. Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid. J Biol Chem 272 (1997), 18982–18989.
61. 61 Csiszar, A., Lehoux, S., Ungvari, Z., Hemodynamic forces, vascular oxidative stress, and regulation of BMP-2/4 expression. Antioxid Redox Signal 11 (2009), 1683–1697.
62. 62 Liberman, M., Johnson, R.C., Handy, D.E., et al. Bone morphogenetic protein-2 activates NADPH oxidase to increase endoplasmic reticulum stress and human coronary artery smooth muscle cell calcification. Biochem Biophys Res Commun 413 (2011), 436–441.
63. 63 Byon, C.H., Javed, A., Dai, Q., et al. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem 283 (2008), 15319–15327.
64. 64 Skulachev, V.P., Anisimov, V.N., Antonenko, Y.N., et al. An attempt to prevent senescence: a mitochondrial approach. Biochim Biophys Acta 1787 (2009), 437–461.
65. 65 Lauzier, M.C., Page, E.L., Michaud, M.D., Richard, D.E., Differential regulation of hypoxia-inducible factor-1 through receptor tyrosine kinase transactivation in vascular smooth muscle cells. Endocrinology 148 (2007), 4023–4031.
66. 66 Lauzier, M.C., Robitaille, G.A., Chan, D.A., et al. (2R)-[(4-Biphenylylsulfonyl)amino]-N-hydroxy-3-phenylpropionamide (BiPS), a matrix metalloprotease inhibitor, is a novel and potent activator of hypoxia-inducible factors. Mol Pharmacol 74 (2008), 282–288.
67. 67 Lebel, M., Rodrigue, M.E., Agharazii, M., Lariviere, R., Antihypertensive and renal protective effects of renin-angiotensin system blockade in uremic rats treated with erythropoietin. Am J Hypertens 19 (2006), 1286–1292.
68. 68 Owens, G.K., Loeb, A., Gordon, D., Thompson, M.M., Expression of smooth muscle-specific alpha-isoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation. J Cell Biol 102 (1986), 343–352.
69. 69 Block, G.A., Prevalence and clinical consequences of elevated Ca x P product in hemodialysis patients. Clin Nephrol 54 (2000), 318–324.
70. 70 Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J Biol Chem 193 (1951), 265–275.
71. 71 Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 29, 2001, e45.