Inhibition of bone morphogenetic protein signal transduction prevents the medial vascular calcification associated with matrix gla protein deficiency

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Malhotra, Rajeev ^a   Burke, Megan F ^a   Martyn, Trejeeve ^b   Shakartzi, Hannah R ^b   Thayer, Timothy E ^a   O'Rourke, Caitlin ^b   Li, Pingcheng ^b   Derwall, Matthias ^b,c   Spagnolli, Ester ^b   Kolodziej, Starsha A ^b   Hoeft, Konrad ^b   Mayeur, Claire ^b   Jiramongkolchai, Pawina ^b   Kumar, Ravindra ^d   Buys, Emmanuel S ^b   Yu, Paul B ^e   Bloch, Kenneth D ^a,b   Bloch, Donald B ^b,f  

^a Division of Cardiology   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d Acceleron Pharma Inc   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f Division of Rheumatology Immunology and Allergy   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; INHIBITOR OF DIFFERENTIATION 1; MESSENGER RNA; OSTEOCALCIN; SMAD1 PROTEIN; SMAD5 PROTEIN; TRANSCRIPTION FACTOR RUNX2; 6 [4 (1 PIPERAZINYL)PHENYL] 3 (4 QUINOLINYL)PYRAZOLO[1,5 A]PYRIMIDINE; CALCIUM BINDING PROTEIN; MATRIX GLA PROTEIN; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; SCLEROPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY CALCIFICATION; ARTICLE; BLOOD VESSEL CALCIFICATION; BONE DEVELOPMENT; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DISEASE ASSOCIATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION; ID1 GENE; INTRACELLULAR SIGNALING; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OPN GENE; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RUNX2 GENE; SIGNAL TRANSDUCTION; SURVIVAL TIME; WILD TYPE MOUSE; ANIMAL; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; KNOCKOUT MOUSE; METABOLISM; VASCULAR CALCIFICATION;

ANIMALIA; MUS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CALCIUM-BINDING PROTEINS; EXTRACELLULAR MATRIX PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, KNOCKOUT; PYRAZOLES; PYRIMIDINES; SIGNAL TRANSDUCTION; VASCULAR CALCIFICATION;

EID: 84928969296     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117098     Document Type: Article

References (54)

1. Abedin M, Tintut Y, Demer LL (2004) Vascular calcification: mechanisms and clinical ramifications. ArteriosclerThromb Vasc Biol 24:1161-1170. doi: 10.1161/01. ATV.0000133194.94939.42 PMID: 15155384
2. Huang H, Virmani R, Younis H, Burke AP, Kamm RD, etal. (2001) The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 103:1051-1056. doi: 10.1161/01. CIR.103. 8.1051 PMID: 11222465
3. Vengrenyuk Y, Carlier S, Xanthos S, Cardoso L, Ganatos P, etal. (2006) A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci U S A 103:14678-14683. doi: 10.1073/pnas.0606310103 PMID: 17003118
4. Virmani R, Burke AP, Farb A, Kolodgie FD (2006) Pathology of the vulnerable plaque. J Am Coll Cardiol 47:C13-18. doi: 10.1016/j.jacc.2005.10.065 PMID: 16631505
5. Amann K (2008) Media calcification and intima calcification are distinct entities in chronic kidney disease. Clin J Am Soc Nephrol 3:1599-1605. doi: 10.2215/CJN.02120508 PMID: 18815240
6. Otsuka F, Sakakura K, Yahagi K, Joner M, Virmani R (2014) Has our understanding of calcification in human coronary atherosclerosis progressed? ArteriosclerThromb Vasc Biol 34:724-736. doi: 10.1161/ATVBAHA.113.302642 PMID: 24558104
7. Hruska KA, Mathew S, Saab G (2005) Bone morphogenetic proteins in vascular calcification. Circ Res 97:105-114. doi: 10.1161/01. RES.00000175571.53833.6c PMID: 16037577
8. Vattikuti R, Towler DA (2004) Osteogenic regulation of vascular calcification: an early perspective. Am J Physiol Endocrinol Metab 286:E686-696. doi: 10.1152/ajpendo.00552.2003 PMID: 15102615
9. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, etal. (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386:78-81. doi: 10.1038/386078a0 PMID: 9052783
10. Keutel J, Jorgensen G, Gabriel P (1971) [A new autosomal-recessive hereditary syndrome. Multiple peripheral pulmonary stenosis, brachytelephalangia, inner-ear deafness, ossification or calcification of cartilages]. Dtsch Med Wochenschr 96:1676-1681 passim. doi: 10.1055/s-0028-1110200 PMID: 5099199
11. Munroe PB, Olgunturk RO, Fryns JP, Van Maldergem L, Ziereisen F, etal. (1999) Mutations in the gene encoding the human matrix Gla protein cause Keutel syndrome. Nat Genet 21:142-144. doi: 10.1038/5102 PMID: 9916809
12. Meier M, Weng LP, Alexandrakis E, Ruschoff J, Goeckenjan G (2001) Tracheobronchial stenosis in Keutel syndrome. EurRespirJ 17:566-569. doi: 10.1183/09031936.01.17305660 PMID: 11405537
13. Proudfoot D, Shanahan CM (2006) Molecular mechanisms mediating vascular calcification: role of matrix Gla protein. Nephrology (Carlton) 11:455-461. doi: 10.1111/j.1440-1797.2006.00660.x
14. Crosier MD, Booth SL, Peter I, Dawson-Hughes B, Price PA, etal. (2009) Matrix Gla protein polymorphisms are associated with coronary artery calcification in men. J Nutr Sci Vitaminol (Tokyo) 55:59-65. doi: 10.3177/jnsv. 55.59
15. Cassidy-Bushrow AE, Bielak LF, Levin AM, Sheedy PF 2nd, Turner ST, etal. (2013) Matrix gla protein gene polymorphism is associated with increased coronary artery calcification progression. Arterioscler Thromb Vasc Biol 33:645-651. doi: 10.1161/ATVBAHA.112.300491 PMID: 23307874
16. Johnson RC, Leopold JA, Loscalzo J (2006) Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res 99:1044-1059. doi: 10.1161/01. RES.0000249379.55535.21 PMID: 17095733
17. O'Young J, Liao Y, Xiao Y, Jalkanen J, Lajoie G, etal. (2011) Matrix Gla protein inhibits ectopic calcification by a direct interaction with hydroxyapatite crystals. J AmChemSoc 133:18406-18412. doi: 10.1021/ja207628k PMID: 21961692
18. Yagami K, Suh JY, Enomoto-Iwamoto M, Koyama E, Abrams WR, et al. (1999) Matrix GLA protein is a developmental regulator of chondrocyte mineralization and, when constitutively expressed, blocks endochondral and intramembranous ossification in the limb. J Cell Biol 147:1097-1108. doi: 10.1083/jcb. 147.5.1097 PMID: 10579728
19. Lomashvili KA, Wang X, Wallin R, O'Neill WC (2011) Matrix Gla protein metabolism in vascular smooth muscle and role in uremic vascular calcification. J Biol Chem 286:28715-28722. doi: 10.1074/jbc. M111.251462 PMID: 21705322
20. Roy ME, Nishimoto SK (2002) Matrix Gla protein binding to hydroxyapatite is dependent on the ionic environment: calcium enhances binding affinity but phosphate and magnesium decrease affinity. Bone 31:296-302. doi: 10.1016/S8756-3282 (02) 00821-9 PMID: 12151082
21. Schurgers LJ, Uitto J, Reutelingsperger CP (2013) Vitamin K-dependent carboxylation of matrix Glaprotein: a crucial switch to control ectopic mineralization. Trends Mol Med 19:217-226. doi: 10.1016/j. molmed.2012.12.008 PMID: 23375872
22. Goiko M, Dierolf J, Gleberzon JS, Liao Y, Grohe B, etal. (2013) Peptides of matrix gla protein inhibit nucleation and growth of hydroxyapatite and calcium oxalate monohydrate crystals. PLoS One 8:e80344. doi: 10.1371/journal.pone.0080344 PMID: 24265810
23. Yao Y, Zebboudj AF, Shao E, Perez M, Bostrom K (2006) Regulation of bone morphogenetic protein-4 by matrix GLA protein in vascular endothelial cells involves activin-like kinase receptor 1. J Biol Chem 281:33921-33930. doi: 10.1074/jbc. M604239200 PMID: 16950789
24. Zebboudj AF, Imura M, Bostrom K (2002) Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2. J Biol Chem 277:4388-4394. doi: 10.1074/jbc. M109683200 PMID: 11741887
25. Wallin R, Cain D, Hutson SM, Sane DC, Loeser R (2000) Modulation of the binding of matrix Gla protein (MGP) to bone morphogenetic protein-2 (BMP-2). Thromb Haemost 84:1039-1044. PMID: 11154111
26. Cai J, Pardali E, Sanchez-Duffhues G, ten Dijke P (2012) BMP signaling in vascular diseases. FEBS Lett 586:1993-2002. doi: 10.1016/j.febslet.2012.04.030 PMID: 22710160
27. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, etal. (2011) Bone morphogenetic proteins: a critical review. Cell Signal 23:609-620. doi: 10.1016/j.cellsig.2010.10.003 PMID: 20959140
28. Abe E, Yamamoto M, Taguchi Y, Lecka-Czernik B, O'Brien CA, et al. (2000) Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by noggin. Journal of bone and mineral research: the official journal of the American Society for Bone and Mineral Research 15:663-673. doi: 10.1359/jbmr.2000.15.4.663
29. Bostrom K, Watson KE, Horn S, Wortham C, Herman IM, etal. (1993) Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest 91:1800-1809. doi: 10.1172/JCI116391 PMID: 8473518
30. Nakagawa Y, Ikeda K, Akakabe Y, Koide M, Uraoka M, etal. (2010) Paracrine osteogenic signals via bone morphogenetic protein-2 accelerate the atherosclerotic intimal calcification in vivo. Arterioscler Thromb Vasc Biol 30:1908-1915. doi: 10.1161/ATVBAHA.110.206185 PMID: 20651281
31. Derwall M, Malhotra R, Lai CS, Beppu Y, Aikawa E, etal. (2012) Inhibition of bone morphogenetic protein signaling reduces vascular calcification and atherosclerosis. Arterioscler Thromb Vasc Biol 32:613-622. doi: 10.1161/ATVBAHA.111.242594 PMID: 22223731
32. Hedin U, Roy J, Tran PK, Lundmark K, Rahman A (1999) Control of smooth muscle cell proliferationthe role of the basement membrane. Thromb Haemost 82 Suppl 1:23-26.
33. Sage AP, Tintut Y, Demer LL (2010) Regulatory mechanisms in vascular calcification. Nat Rev Cardiol 7:528-536. doi: 10.1038/nrcardio.2010.115 PMID: 20664518
34. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, etal. (2000) Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell lineC2C12. Mol Cell Biol 20:8783-8792. doi: 10.1128/MCB.20.23.8783-8792.2000 PMID: 11073979
35. Rusanescu G, Weissleder R, Aikawa E (2008) Notch signaling in cardiovascular disease and calcification. Curr Cardiol Rev 4:148-156. doi: 10.2174/157340308785160552 PMID: 19936191
36. Matsubara T, Kida K, Yamaguchi A, Hata K, Ichida F, et al. (2008) BMP2 regulates Osterix through Msx2and Runx2 during osteoblast differentiation. J Biol Chem 283:29119-29125. doi: 10.1074/jbc. M801774200 PMID: 18703512
37. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, etal. (2001) Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res 89:1147-1154. doi: 10.1161/hh2401.101070 PMID: 11739279
38. Speer MY, Li X, Hiremath PG, Giachelli CM (2010) Runx2/Cbfa1, but not loss of myocardin, is required for smooth muscle cell lineage reprogramming toward osteochondrogenesis. J Cell Biochem 110:935-947. doi: 10.1002/jcb.22607 PMID: 20564193
39. Speer MY, McKee MD, Guldberg RE, Liaw L, Yang HY, etal. (2002) Inactivation of the osteopontin gene enhances vascular calcification of matrix Gla protein-deficient mice: evidence for osteopontin as an inducible inhibitor of vascular calcification in vivo. J Exp Med 196:1047-1055. doi: 10.1084/jem. 20020911 PMID: 12391016
40. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, etal. (2008) Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem 283:15319-15327. doi: 10.1074/jbc. M800021200 PMID: 18378684
41. Speer MY, Yang HY, Brabb T, Leaf E, Look A, etal. (2009) Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res 104:733-741. doi: 10.1161/CIRCRESAHA.108.183053 PMID: 19197075
42. Yao Y, Jumabay M, Ly A, Radparvar M, Cubberly MR, etal. (2013) A role for the endothelium in vascular calcification. Circ Res 113:495-504. doi: 10.1161/CIRCRESAHA.113.301792 PMID: 23852538
43. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, etal. (2010) Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16:1400-1406. doi: 10.1038/nm.2252 PMID: 21102460
44. Cuny GD, Yu PB, Laha JK, Xing X, Liu JF, etal. (2008) Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg Med Chem Lett 18:4388-4392. doi: 10.1016/j.bmcl.2008.06.052 PMID: 18621530
45. Aikawa E, Nahrendorf M, Figueiredo JL, Swirski FK, Shtatland T, et al. (2007) Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation 116:2841-2850. doi: 10.1161/CIRCULATIONAHA.107.732867 PMID: 18040026
46. Aikawa E, Nahrendorf M, Sosnovik D, Lok VM, Jaffer FA, etal. (2007) Multimodality molecular imaging identifies proteolytic and osteogenic activities in early aortic valve disease. Circulation 115:377-386. doi: 10.1161/CIRCULATIONAHA.106.654913 PMID: 17224478
47. Rong JX, Shapiro M, Trogan E, Fisher EA (2003) Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci USA 100:13531-13536. doi: 10.1073/pnas.1735526100 PMID: 14581613
48. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acidguanidiniumthiocyanatephenol-chloroformextraction. Anal Biochem 162:156-159. doi: 10.1016/0003-2697 (87) 90021-2 PMID: 2440339
49. Luo J, Deng ZL, Luo X, Tang N, Song WX, etal. (2007) A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. NatProtoc 2:1236-1247. doi: 10.1038/nprot.2007.135 PMID: 17546019
50. Yao Y, Bennett BJ, Wang X, Rosenfeld ME, Giachelli C, etal. (2010) Inhibition of Bone Morphogenetic Proteins Protects Against Atherosclerosis and Vascular Calcification. Circ Res 107:485-494. doi: 10.1161/CIRCRESAHA.110.219071 PMID: 20576934
51. Zebboudj AF, Shin V, Bostrom K (2003) Matrix GLA protein and BMP-2 regulate osteoinduction in calcifying vascular cells. J Cell Biochem 90:756-765. doi: 10.1002/jcb.10669 PMID: 14587031
52. Shao JS, Cai J, Towler DA (2006) Molecular mechanisms of vascular calcification: lessons learned from the aorta. ArteriosclerThromb Vasc Biol 26:1423-1430. doi: 10.1161/01. ATV.0000220441. 42041.20 PMID: 16601233
53. Sun Y, Byon CH, Yuan K, Chen J, Mao X, etal. (2012) Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification. Circ Res 111:543-552. doi: 10.1161/CIRCRESAHA.112.267237 PMID: 22773442
54. Boskey AL, Maresca M, Ullrich W, Doty SB, Butler WT, etal. (1993) Osteopontin-hydroxyapatite interactions in vitro: inhibition of hydroxyapatite formation and growth in a gelatin-gel. Bone Miner 22:147-159. doi: 10.1016/S0169-6009 (08) 80225-5 PMID: 8251766