Transglutaminase inhibitors attenuate vascular calcification in a preclinical model

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 1, 2013, Pages 43-51

  Beazley, Kelly E ^a   Banyard, Derek ^a   Lima, Florence ^a   Deasey, Stephanie C ^a   Nurminsky, Dmitry I ^a   Konoplyannikov, Mikhail ^a   Nurminskaya, Maria V ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

catenin; quercetin; transglutaminase 2; vascular calcification; warfarin

Indexed keywords

ACYLTRANSFERASE INHIBITOR; BETA CATENIN; KCC 009; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; QU 995; QUERCETIN; UNCLASSIFIED DRUG; WARFARIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA MEDIA; ARTICLE; BLOOD VESSEL CALCIFICATION; BLOOD VESSEL WALL; CONTROLLED STUDY; IN VITRO STUDY; MALE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYSTOLIC HYPERTENSION;

ANIMALS; AORTA; AORTIC DISEASES; BETA CATENIN; BLOOD PRESSURE; CELL LINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; GTP-BINDING PROTEINS; ISOXAZOLES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; OSTEOGENESIS; PHOSPHORYLATION; QUERCETIN; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TRANSGLUTAMINASES; VASCULAR CALCIFICATION; WARFARIN;

EID: 84871821231     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300260     Document Type: Article

References (54)

1. Caira FC, Stock SR, Gleason TG, McGee EC, Huang J, Bonow RO, Spelsberg TC, McCarthy PM, Rahimtoola SH, Rajamannan NM. Human degenerative valve disease is associated with up-regulation of low-density lipoprotein receptor-related protein 5 receptor-mediated bone formation. J Am Coll Cardiol. 2006;47:1707-1712.
2. Iyemere VP, Proudfoot D, Weissberg PL, Shanahan CM. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J Intern Med. 2006;260:192-210.
3. Demer LL, Tintut Y. Vascular calcification: pathobiology of a multifaceted disease. Circulation. 2008;117:2938-2948.
4. Speer MY, Yang HY, Brabb T, Leaf E, Look A, Lin WL, Frutkin A, Dichek D, Giachelli CM. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res. 2009;104:733-741.
5. London GM. Cardiovascular calcifications in uremic patients: clinical impact on cardiovascular function. J Am Soc Nephrol. 2003;14(9 Suppl 4):S305-S309.
6. Moe SM, Reslerova M, Ketteler M, O'neill K, Duan D, Koczman J, Westenfeld R, Jahnen-Dechent W, Chen NX. Role of calcification inhibitors in the pathogenesis of vascular calcification in chronic kidney disease (CKD). Kidney Int. 2005;67:2295-2304.
7. Dao HH, Essalihi R, Graillon JF, Larivière R, De Champlain J, Moreau P. Pharmacological prevention and regression of arterial remodeling in a rat model of isolated systolic hypertension. J Hypertens. 2002;20:1597-1606.
8. Price PA, Faus SA, Williamson MK. Warfarin causes rapid calcification of the elastic lamellae in rat arteries and heart valves. Arterioscler Thromb Vasc Biol. 1998;18:1400-1407.
9. Palaniswamy C, Sekhri A, Aronow WS, Kalra A, Peterson SJ. Association of warfarin use with valvular and vascular calcification: a review. Clin Cardiol. 2011;34:74-81.
10. Chatrou ML, Winckers K, Hackeng TM, Reutelingsperger CP, Schurgers LJ. Vascular calcification: the price to pay for anticoagulation therapy with vitamin K-antagonists. Blood Rev. 2012;26:155-166.
11. 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.
12. 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.
13. Lomashvili KA, Wang X, Wallin R, O'Neill WC. Matrix Gla protein metabolism in vascular smooth muscle and role in uremic vascular calcification. J Biol Chem. 2011;286:28715-28722.
14. Boström KI, Rajamannan NM, Towler DA. The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ Res. 2011;109:564-577.
15. Long F. Targeting intercellular signals for bone regeneration from bone marrow mesenchymal progenitors. Cell Cycle. 2008;7:2106-2111.
16. Schurgers LJ, Spronk HM, Soute BA, Schiffers PM, DeMey JG, Vermeer C. Regression of warfarin-induced medial elastocalcinosis by high intake of vitamin K in rats. Blood. 2007;109:2823-2831.
17. Beazley KE, Deasey S, Lima F, Nurminskaya MV. Transglutaminase 2-mediated activation of β-catenin signaling has a critical role in warfarin-induced vascular calcification. Arterioscler Thromb Vasc Biol. 2012;32:123-130.
18. Faverman L, Mikhaylova L, Malmquist J, Nurminskaya M. Extracellular transglutaminase 2 activates beta-catenin signaling in calcifying vascular smooth muscle cells. FEBS Lett. 2008;582:1552-1557.
19. Hendrickx M, Leyns L. Non-conventional Frizzled ligands and Wnt receptors. Dev Growth Differ. 2008;50:229-243.
20. Watts RE, Siegel M, Khosla C. Structure-activity relationship analysis of the selective inhibition of transglutaminase 2 by dihydroisoxazoles. J Med Chem. 2006;49:7493-7501.
21. Park CH, Chang JY, Hahm ER, Park S, Kim HK, Yang CH. Quercetin, a potent inhibitor against beta-catenin/Tcf signaling in SW480 colon cancer cells. Biochem Biophys Res Commun. 2005;328:227-234.
22. Han W, Wang W, Mohammed KA, Su Y. Alpha-defensins increase lung fibroblast proliferation and collagen synthesis via the beta-catenin signaling pathway. FEBS J. 2009;276:6603-6614.
23. Shan BE, Wang MX, Li RQ. Quercetin inhibit human SW480 colon cancer growth in association with inhibition of cyclin D1 and survivin expression through Wnt/beta-catenin signaling pathway. Cancer Invest. 2009;27:604-612.
24. Essalihi R, Dao HH, Yamaguchi N, Moreau P. A new model of isolated systolic hypertension induced by chronic warfarin and vitamin K1 treatment. Am J Hypertens. 2003;16:103-110.
25. Prosdocimo DA, Wyler SC, Romani AM, O'Neill WC, Dubyak GR. Regulation of vascular smooth muscle cell calcification by extracellular pyrophosphate homeostasis: synergistic modulation by cyclic AMP and hyperphosphatemia. Am J Physiol, Cell Physiol. 2010;298:C702-C713.
26. Cheng SL, Shao JS, Halstead LR, Distelhorst K, Sierra O, Towler DA. Activation of vascular smooth muscle parathyroid hormone receptor inhibits Wnt/beta-catenin signaling and aortic fibrosis in diabetic arteriosclerosis. Circ Res. 2010;107:271-282.
27. Chabot N, Moreau S, Mulani A, Moreau P, Keillor JW. Fluorescent probes of tissue transglutaminase reveal its association with arterial stiffening. Chem Biol. 2010;17:1143-1150.
28. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem. 2006;281:22429-22433.
29. 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. 2011;31:e55-e71.
30. Makabe S, Takahashi Y, Watanabe H, Murakami M, Ohba T, Ito H. Fluvastatin protects vascular smooth muscle cells against oxidative stress through the Nrf2-dependent antioxidant pathway. Atherosclerosis. 2010;213:377-384.
31. Montecucco F, Steffens S, Mach F. The immune response is involved in atherosclerotic plaque calcification: could the RANKL/RANK/OPG system be a marker of plaque instability? Clin Dev Immunol. 2007;2007:75805.
32. Di Bari L, Ripoli S, Pradhan S, Salvadori P. Interactions between quercetin and warfarin for albumin binding: a new eye on food/drug interference. Chirality. 2010;22:593-596.
33. Notoya M, Tsukamoto Y, Nishimura H, Woo JT, Nagai K, Lee IS, Hagiwara H. Quercetin, a flavonoid, inhibits the proliferation, differentiation, and mineralization of osteoblasts in vitro. Eur J Pharmacol. 2004;485:89-96.
34. Terao J, Kawai Y, Murota K. Vegetable flavonoids and cardiovascular disease. Asia Pac J Clin Nutr. 2008;17:291-293.
35. Giachelli CM. Inducers and inhibitors of biomineralization: lessons from pathological calcification. Orthod Craniofac Res. 2005;8:229-231.
36. Rusanescu G, Weissleder R, Aikawa E. Notch signaling in cardiovascular disease and calcification. Curr Cardiol Rev. 2008;4:148-156.
37. Beazley KE, Zhang T, Lima F, Pozharskaya T, Niger C, Tzitzikov E, Azimzadeh AM, Nurminskaya M. Implication for transglutaminase 2-mediated activation of β-catenin signaling in neointimal vascular smooth muscle cells in chronic cardiac allograft rejection. J Heart Lung Transplant. 2012;31:1009-1017.
38. Zhai W, Lü X, Chang J, Zhou Y, Zhang H. Quercetin-crosslinked porcine heart valve matrix: mechanical properties, stability, anticalcification and cytocompatibility. Acta Biomater. 2010;6:389-395.
39. Harwood M, Danielewska-Nikiel B, Borzelleca JF, Flamm GW, Williams GM, Lines TC. A critical review of the data related to the safety of quercetin and lack of evidence of in vivo toxicity, including lack of genotoxic/carcinogenic properties. Food Chem Toxicol. 2007;45:2179-2205.
40. Johnson KA, Polewski M, Terkeltaub RA. Transglutaminase 2 is central to induction of the arterial calcification program by smooth muscle cells. Circ Res. 2008;102:529-537.
41. Deasey S, Shanmugasundaram S, Nurminskaya M. Tissue-specific responses to loss of transglutaminase 2. Amino Acids. 2011. doi: 10.1007/s00726-011-1183-9. http://www.springerlink.com/content/n2uqx02484233832/. Accessed November 5, 2012.
42. Johnson KB, Petersen-Jones H, Thompson JM, Hitomi K, Itoh M, Bakker EN, Johnson GV, Colak G, Watts SW. Vena cava and aortic smooth muscle cells express transglutaminases 1 and 4 in addition to transglutaminase 2. Am J Physiol Heart Circ Physiol. 2012;302:H1355-H1366.
43. Matlung HL, Groen HC, de Vos J, van Walsum T, van der Lugt A, Niessen WJ, Wentzel JJ, Vanbavel E, Bakker EN. Calcification locates to transglutaminases in advanced human atherosclerotic lesions. Am J Pathol. 2009;175:1374-1379.
44. Bakker EN, Pistea A, VanBavel E. Transglutaminases in vascular biology: relevance for vascular remodeling and atherosclerosis. J Vasc Res. 2008;45:271-278.
45. Santhanam L, Tuday EC, Webb AK, et al. Decreased S-nitrosylation of tissue transglutaminase contributes to age-related increases in vascular stiffness. Circ Res. 2010;107:117-125.
46. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
47. Kleemann R, Verschuren L, Morrison M, Zadelaar S, van Erk MJ, Wielinga PY, Kooistra T. Anti-inflammatory, anti-proliferative and anti-atherosclerotic effects of quercetin in human in vitro and in vivo models. Atherosclerosis. 2011;218:44-52.
48. Edwards RL, Lyon T, Litwin SE, Rabovsky A, Symons JD, Jalili T. Quercetin reduces blood pressure in hypertensive subjects. J Nutr. 2007;137:2405-2411.
49. Egert S, Bosy-Westphal A, Seiberl J, Kürbitz C, Settler U, Plachta-Danielzik S, Wagner AE, Frank J, Schrezenmeir J, Rimbach G, Wolffram S, Müller MJ. Quercetin reduces systolic blood pressure and plasma oxidised low-density lipoprotein concentrations in overweight subjects with a high-cardiovascular disease risk phenotype: a double-blinded, placebo-controlled cross-over study. Br J Nutr. 2009;102:1065-1074.
50. Huxley RR, Neil HA. The relation between dietary flavonol intake and coronary heart disease mortality: a meta-analysis of prospective cohort studies. Eur J Clin Nutr. 2003;57:904-908.
51. Shao JS, Cheng SL, Pingsterhaus JM, Charlton-Kachigian N, Loewy AP, Towler DA. Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J Clin Invest. 2005;115:1210-1220.
52. Murshed M, Schinke T, McKee MD, Karsenty G. Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol. 2004;165:625-630.
53. Shea MK, O'Donnell CJ, Vermeer C, Magdeleyns EJ, Crosier MD, Gundberg CM, Ordovas JM, Kritchevsky SB, Booth SL. Circulating uncarboxylated matrix gla protein is associated with vitamin K nutritional status, but not coronary artery calcium, in older adults. J Nutr. 2011;141:1529-1534.
54. Nasir K, Roguin A, Sarwar A, Rumberger JA, Blumenthal RS. Gender differences in coronary arteries and thoracic aorta calcification. Arterioscler Thromb Vasc Biol. 2007;27:1220-1222.