Pathophysiological role of vascular smooth muscle alkaline phosphatase in medial artery calcification

Journal of Bone and Mineral Research

Volumn 30, Issue 5, 2015, Pages 824-836

  Sheen, Campbell R ^a   Kuss, Pia ^a   Narisawa, Sonoko ^a   Yadav, Manisha C ^a   Nigro, Jessica ^a   Wang, Wei ^a   Chhea, T Nicole ^a   Sergienko, Eduard A ^a   Kapoor, Kapil ^a   Jackson, Michael R ^a   Hoylaerts, Marc F ^b   Pinkerton, Anthony B ^a   O'Neill, W Charles ^c   Millán, José Luis ^a  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Genetic animal models; Matrix mineralization; Preclinical studies; Therapeutics

Indexed keywords

ACAN PROTEIN; ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; ANK PROTEIN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM; COLLAGEN TYPE 1 A1; CRE RECOMBINASE; ECTONUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE 1; ESTERASE INHIBITOR; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MATRIX GLA PROTEIN; OSTEOCALCIN; OSTEOPONTIN; PHOSPHO1 PROTEIN; PHOSPHORUS; SBI 425; SLC20A1 PROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; TRANSGELIN; UNCLASSIFIED DRUG; ALKALINE PHOSPHATASE 2, MOUSE; ENZYME INHIBITOR; MESSENGER RNA;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTERY CALCIFICATION; ARTICLE; CARDIOMEGALY; CARDIOVASCULAR FUNCTION; CARTILAGE CELL; CELL TRANSDIFFERENTIATION; COLORIMETRY; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DOWN REGULATION; DRUG BLOOD LEVEL; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HEART LEFT VENTRICLE HYPERTROPHY; HEART LEFT VENTRICLE MASS; HEART SIZE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HYPERTENSION; IN VITRO STUDY; LIFE EXPECTANCY; M MODE ECHOCARDIOGRAPHY; MALE; MEDIAL ARTERY CALCIFICATION; MOUSE; NICK END LABELING; NONHUMAN; OSTEOBLAST; PATHOPHYSIOLOGY; PHENOTYPE; PROGENY; SYSTOLIC BLOOD PRESSURE; UPREGULATION; VASCULAR SMOOTH MUSCLE; X CHROMOSOME; X CHROMOSOME INACTIVATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; BLOOD VESSEL CALCIFICATION; CHEMISTRY; DIAGNOSTIC IMAGING; DRUG EFFECTS; ECHOGRAPHY; ENZYMOLOGY; GENETICS; METABOLISM; NEWBORN; PATHOLOGY; TRANSGENIC MOUSE; TREATMENT OUTCOME;

ALKALINE PHOSPHATASE; ANIMALS; ANIMALS, NEWBORN; AORTA; ENZYME INHIBITORS; MALE; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; RNA, MESSENGER; TREATMENT OUTCOME; ULTRASONOGRAPHY; VASCULAR CALCIFICATION;

EID: 84927747550     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2420     Document Type: Article

References (60)

1. Blacher J, Guerin AP, Pannier B, Marchais SJ, London GM,. Arterial calcifications, arterial stiffness, and cardiovascular risk in end-stage renal disease. Hypertension. 2001; 38 (4): 938-942.
2. Witteman JC, Kok FJ, van Saase JL, Valkenburg HA,. Aortic calcification as a predictor of cardiovascular mortality. Lancet. 1986; 2 (8516): 1120-1122.
3. Towler DA,. Vascular calcification: a perspective on an imminent disease epidemic. IBMS BoneKEy. 2008; 5 (2): 41-58.
4. Towler DA, Demer LL,. Thematic series on the pathobiology of vascular calcification: an introduction. Circ Res. 2011; 108 (11): 1378-1380.
5. McEniery CM, McDonnell BJ, So A, et al. Aortic calcification is associated with aortic stiffness and isolated systolic hypertension in healthy individuals. Hypertension. 2009; 53 (3): 524-531.
6. Lehto S, Niskanen L, Suhonen M, Ronnemaa T, Laakso M,. Medial artery calcification. A neglected harbinger of cardiovascular complications in non-insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol. 1996; 16 (8): 978-983.
7. 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 (9): 1731-1740.
8. Sutliff RL, Walp ER, El-Ali AM, et al. Effect of medial calcification on vascular function in uremia. Am J Physiol Renal Physiol. 2011; 301 (1): F78-F83.
9. Rutsch F, Ruf N, Vaingankar S, et al. Mutations in ENPP1 are associated with 'idiopathic' infantile arterial calcification. Nat Genet. 2003; 34 (4): 379-381.
10. St Hilaire C, Ziegler SG, Markello TC, et al. NT5E mutations and arterial calcifications. N Engl J Med. 2011; 364 (5): 432-442.
11. Nitschke Y, Rutsch F,. Generalized arterial calcification of infancy and pseudoxanthoma elasticum: two sides of the same coin. Front Genet. 2012; 3: 302.
12. Sallam T, Cheng H, Demer LL, Tintut Y,. Regulatory circuits controlling vascular cell calcification. Cell Mol Life Sci. 2013; 70 (17): 3187-3197.
13. El-Maadawy S, Kaartinen MT, Schinke T, et al. Cartilage formation and calcification in arteries of mice lacking matrix Gla protein. Connect Tissue Res. 2003; 44 (Suppl 1): 272-278.
14. Schafer C, Heiss A, Schwarz A, et al. The serum protein alpha 2-Heremans-Schmid glycoprotein/fetuin-A is a systemically acting inhibitor of ectopic calcification. J Clin Invest. 2003; 112 (3): 357-366.
15. Meyer JL,. Can biological calcification occur in the presence of pyrophosphate. Arch Biochem Biophys. 1984; 231 (1): 1-8.
16. Whyte MP, Greenberg CR, Salman NJ, et al. Enzyme-replacement therapy in life-threatening hypophosphatasia. N Engl J Med. 2012; 366 (10): 904-913.
17. Narisawa S, Frohlander N, Millan JL,. Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn. 1997; 208 (3): 432-446.
18. Fedde KN, Blair L, Silverstein J, et al. Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J Bone Miner Res. 1999; 14 (12): 2015-2026.
19. Hessle L, Johnson KA, Anderson HC, et al. Tissue-nonspecific alkaline phosphatase,plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci USA. 2002; 99 (14): 9445-9449.
20. Millan JL, Narisawa S, Lemire I, et al. Enzyme replacement therapy for murine hypophosphatasia. J Bone Miner Res. 2008; 23 (6): 777-787.
21. Shanahan CM, Cary NR, Salisbury JR, et al. Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation. 1999; 100 (21): 2168-2176.
22. Moe SM, Duan D, Doehle BP, O'Neill KD, Chen NX,. Uremia induces the osteoblast differentiation factor Cbfa1 in human blood vessels. Kidney Int. 2003; 63 (3): 1003-1011.
23. Shroff RC, McNair R, Figg N, et al. Dialysis accelerates medial vascular calcification in part by triggering smooth muscle cell apoptosis. Circulation. 2008; 118 (17): 1748-1757.
24. Lomashvili KA, Garg P, Narisawa S, Millan JL, O'Neill WC,. Upregulation of alkaline phosphatase and pyrophosphate hydrolysis: potential mechanism for uremic vascular calcification. Kidney Int. 2008; 73 (9): 1024-1030.
25. Ren X, Wei Q, Shao H, Sun Z, Liu N,. A rat model of diabetic artery calcification. J Endocrinol Invest. 2012; 35 (5): 497-503.
26. Villa-Bellosta R, Rivera-Torres J, Osorio FG, et al. Defective extracellular pyrophosphate metabolism promotes vascular calcification in a mouse model of Hutchinson-Gilford progeria syndrome that is ameliorated on pyrophosphate treatment. Circulation. 2013; 127 (24): 2442-2451.
27. Leroux-Berger M, Queguiner I, Maciel TT, et al. Pathologic calcification of adult vascular smooth muscle cells differs on their crest or mesodermal embryonic origin. J Bone Miner Res. 2011; 26 (7): 1543-1553.
28. -/- mice. Arterioscler Thromb Vasc Biol. 2005; 25 (4): 686-691.
29. Narisawa S, Harmey D, Yadav MC, et al. Novel inhibitors of alkaline phosphatase suppress vascular smooth muscle cell calcification. J Bone Miner Res. 2007; 22 (11): 1700-1710.
30. Rutsch F, Vaingankar S, Johnson K, et al. PC-1 nucleoside triphosphate pyrophosphohydrolase deficiency in idiopathic infantile arterial calcification. Am J Pathol. 2001; 158 (2): 543-554.
31. O'Neill WC, Lomashvili KA, Malluche HH, Faugere MC, Riser BL,. Treatment with pyrophosphate inhibits uremic vascular calcification. Kidney Int. 2011; 79 (5): 512-517.
32. Li L, Miano JM, Cserjesi P, Olson EN,. SM22 alpha, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res. 1996; 78 (2): 188-195.
33. Holtwick R, Gotthardt M, Skryabin B, et al. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci USA. 2002; 99 (10): 7142-7147.
34. Johnson K, Vaingankar S, Chen Y, et al. Differential mechanisms of inorganic pyrophosphate production by plasma cell membrane glycoprotein-1 and B10 in chondrocytes. Arthritis Rheum. 1999; 42 (9): 1986-1997.
35. Yadav MC, Huesa C, Narisawa S, et al. Ablation of osteopontin improves the skeletal phenotype of phospho1 mice. J Bone Miner Res. 2014; Nov 29 (11): 2369-2381.
36. Narisawa S, Hofmann MC, Ziomek CA, Millan JL,. Embryonic alkaline phosphatase is expressed at M-phase in the spermatogenic lineage of the mouse. Development. 1992; 116 (1): 159-165.
37. Narisawa S, Yadav MC, Millan JL,. In vivo overexpression of tissue-nonspecific alkaline phosphatase increases skeletal mineralization and affects the phosphorylation status of osteopontin. J Bone Miner Res. 2013; 28 (7): 1587-1598.
38. Moorehead WR, Biggs HG,. 2-Amino-2-methyl-1-propanol as the alkalizing agent in an improved continuous-flow cresolphthalein complexone procedure for calcium in serum. Clin Chem. 1974; 20 (11): 1458-1460.
39. Dahl R, Sergienko EA, Su Y, et al. Discovery and validation of a series of aryl sulfonamides as selective inhibitors of tissue-nonspecific alkaline phosphatase (TNAP). J Med Chem. 2009; 52 (21): 6919-6925.
40. Pinkerton AB, Dahl R, Cosford NDP, Millan JL,. Inventors. Sanford-Burnham Medical Research Institute, assignee. Sulfonamide compounds and uses as TNAP inhibitors. CNY World patent WO 2013/126608. 2013 Feb 21. Available from: http://patentscope.wipo.int/search/en/WO2013126608.
41. Coburn SP, Mahuren JD, Jain M, Zubovic Y, Wortsman J,. Alkaline phosphatase (EC 3.1.3.1) in serum is inhibited by physiological concentrations of inorganic phosphate. J Clin Endocrinol Metab. 1998; 83 (11): 3951-3957.
42. Whyte MP, Valdes R Jr, Ryan LM, McAlister WH,. Infantile hypophosphatasia: enzyme replacement therapy by intravenous infusion of alkaline phosphatase-rich plasma from patients with Paget bone disease. J Pediatr. 1982; 101 (3): 379-386.
43. Whyte MP, McAlister WH, Patton LS, et al. Enzyme replacement therapy for infantile hypophosphatasia attempted by intravenous infusions of alkaline phosphatase-rich Paget plasma: results in three additional patients. J Pediatr. 1984; 105 (6): 926-933.
44. Speer MY, Li X, Hiremath PG, Giachelli CM,. Runx2/Cbfa1, but not loss of myocardin, is required for smooth muscle cell lineage reprogramming toward osteochondrogenesis. J Cell Biochem. 2010; 110 (4): 935-947.
45. Proudfoot D, Shanahan CM,. Nanocrystals seed calcification in more ways than one. Kidney Int. 2011; 79 (4): 379-382.
46. Murshed M, Harmey D, Millan JL, McKee MD, Karsenty G,. Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev. 2005; 19 (9): 1093-1104.
47. Persy VP, McKee MD,. Prevention of vascular calcification: is pyrophosphate therapy a solution. Kidney Int. 2011; 79 (5): 490-493.
48. Li L, Blumenthal DK, Masaki T, Terry CM, Cheung AK,. Differential effects of imatinib on PDGF-induced proliferation and PDGF receptor signaling in human arterial and venous smooth muscle cells. J Cell Biochem. 2006; 99 (6): 1553-1563.
49. Sage AP, Lu J, Tintut Y, Demer LL,. 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 (4): 414-422.
50. Villa-Bellosta R, Wang X, Millan JL, Dubyak GR, O'Neill WC,. Extracellular pyrophosphate metabolism and calcification in vascular smooth muscle. Am J Physiol Heart Circ Physiol. 2011; 301 (1): H61-H68.
51. 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 (1): C210-C220.
52. Towler DA,. Inorganic pyrophosphate: a paracrine regulator of vascular calcification and smooth muscle phenotype. Arterioscler Thromb Vasc Biol. 2005; 25 (4): 651-654.
53. O'Neill WC,. Treatment of vascular calcification. Kidney Int. 2008; 74 (11): 1376-1378.
54. Jung A, Russel RG, Bisaz S, Morgan DB, Fleisch H,. Fate of intravenously injected pyrophosphate-32P in dogs. Am J Physiol. 1970; 218 (6): 1757-1764.
55. Rutsch F, Boyer P, Nitschke Y, et al. Hypophosphatemia, hyperphosphaturia, and bisphosphonate treatment are associated with survival beyond infancy in generalized arterial calcification of infancy. Circ Cardiovasc Genet. 2008; 1 (2): 133-140.
56. Lomashvili KA, Monier-Faugere MC, Wang X, Malluche HH, O'Neill WC,. Effect of bisphosphonates on vascular calcification and bone metabolism in experimental renal failure. Kidney Int. 2009; 75 (6): 617-625.
57. Toussaint ND, Elder GJ, Kerr PG,. Bisphosphonates in chronic kidney disease; balancing potential benefits and adverse effects on bone and soft tissue. Clin J Am Soc Nephrol. 2009; 4 (1): 221-233.
58. Otero JE, Gottesman GS, McAlister WH, et al. Severe skeletal toxicity from protracted etidronate therapy for generalized arterial calcification of infancy. J Bone Miner Res. 2013; 28 (2): 419-430.
59. Sergienko E, Su Y, Chan X, et al. Identification and characterization of novel tissue-nonspecific alkaline phosphatase inhibitors with diverse modes of action. J Biomol Screen. 2009; 14 (7): 824-837.
60. London GM, Pannier B, Guerin AP, et al. Alterations of left ventricular hypertrophy in and survival of patients receiving hemodialysis: follow-up of an interventional study. J Am Soc Nephrol. 2001; 12 (12): 2759-2767.