Increased dietary intake of vitamin a promotes aortic valve calcification in vivo

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 2, 2013, Pages 285-293

  Huk, Danielle J ^a,b,c   Hammond, Harriet L ^a,b   Kegechika, Hiroyuki ^d   Lincoln, Joy ^a,b,e  

^a Center for Cardiovascular and Pulmonary Research   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

all trans retinoic acid; calcific aortic valve disease; extracellular matrix; retinoic acid receptor; retinoic acid response element; retinoid x receptor; vitamin D receptor

Indexed keywords

OSTEOCALCIN; RETINOIC ACID; RETINOID X RECEPTOR; RETINOL PALMITATE; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA VALVE STENOSIS; ARTICLE; BLOOD VESSEL CALCIFICATION; BONE DEVELOPMENT; CALCIFIC AORTIC VALVE DISEASE; CONTROLLED STUDY; DIETARY INTAKE; GENE EXPRESSION; HEART FUNCTION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RETINOL INTOXICATION;

ANIMALS; AORTIC VALVE; CALCINOSIS; CELL LINE; CHICK EMBRYO; COLLAGEN TYPE II; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEART VALVE DISEASES; HYPERVITAMINOSIS A; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOGENESIS; OSTEOPONTIN; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SOX9 TRANSCRIPTION FACTOR; TIME FACTORS; TISSUE CULTURE TECHNIQUES; TRANSFECTION; TRETINOIN; VITAMIN A; VITAMINS;

EID: 84872978085     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300388     Document Type: Article

References (74)

1. Rajamannan NM, Evans FJ, Aikawa E, Grande-Allen KJ, Demer LL, Heistad DD, Simmons CA, Masters KS, Mathieu P, O'Brien KD, Schoen FJ, Towler DA, Yoganathan AP, Otto CM. Calcifc aortic valve disease: not simply a degenerative process: A review and agenda for research from the National Heart and Lung and Blood Institute Aortic Stenosis Working Group. Executive summary: Calcifc aortic valve disease-2011 update. Circulation. 2011;124:1783-1791.
2. Lincoln J, Yutzey KE. Molecular and developmental mechanisms of congenital heart valve disease. Birth Defects Res Part A Clin Mol Teratol. 2011;91:526-534.
3. Cheek JD, Wirrig EE, Alferi CM, James JF, Yutzey KE. Differential activation of valvulogenic, chondrogenic, and osteogenic pathways in mouse models of myxomatous and calcifc aortic valve disease. J Mol Cell Cardiol. 2012;52:689-700.
4. Wirrig EE, Snarr BS, Chintalapudi MR, O'neal JL, Phelps AL, Barth JL, Fresco VM, Kern CB, Mjaatvedt CH, Toole BP, Hoffman S, Trusk TC, Argraves WS, Wessels A. Cartilage link protein 1 (Crtl1), an extracellular matrix component playing an important role in heart development. Dev Biol. 2007;310:291-303.
5. Rajamannan NM, Gersh B, Bonow RO. Calcifc aortic stenosis: from bench to the bedside-emerging clinical and cellular concepts. Heart. 2003;89:801-805.
6. Beckmann E, Grau JB, Sainger R, Poggio P, Ferrari G. Insights into the use of biomarkers in calcifc aortic valve disease. J Heart Valve Dis. 2010;19:441-452.
7. Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes R, King IN, Grossfeld PD, Srivastava D. Mutations in NOTCH1 cause aortic valve disease. Nature. 2005;437:270-274.
8. Freeman RV, Otto CM. Spectrum of calcifc aortic valve disease: pathogen-esis, disease progression, and treatment strategies. Circulation. 2005;111: 3316-3326.
9. Mohler ER 3rd, Wang H, Medenilla E, Scott C. Effect of statin treatment on aortic valve and coronary artery calcifcation. J Heart Valve Dis. 2007;16:378-386.
10. Nus M, MacGrogan D, Martínez-Poveda B, Benito Y, Casanova JC, Fernández-Avilés F, Bermejo J, de la Pompa JL. Diet-induced aortic valve disease in mice haploinsuffcient for the Notch pathway effector RBPJK/CSL. Arterioscler Thromb Vasc Biol. 2011;31:1580-1588.
11. Barrick CJ, Roberts RB, Rojas M, Rajamannan NM, Suitt CB, O'Brien KD, Smyth SS, Threadgill DW. Reduced EGFR causes abnormal valvular differentiation leading to calcifc aortic stenosis and left ventricular hypertrophy in C57BL/6J but not 129S1/SvImJ mice. Am J Physiol Heart Circ Physiol. 2009;297:H65-H75.
12. Nigam V, Srivastava D. Notch1 represses osteogenic pathways in aortic valve cells. J Mol Cell Cardiol. 2009;47:828-834.
13. Aikawa E, Aikawa M, Libby P, Figueiredo JL, Rusanescu G, Iwamoto Y, Fukuda D, Kohler RH, Shi GP, Jaffer FA, Weissleder R. Arterial and aortic valve calcifcation abolished by elastolytic cathepsin S defciency in chronic renal disease. Circulation. 2009;119:1785-1794.
14. Schmidt N, Brandsch C, Kühne H, Thiele A, Hirche F, Stangl GI. Vitamin D receptor defciency and low vitamin D diet stimulate aortic calcifcation and osteogenic key factor expression in mice. PLoS ONE. 2012;7:e35316.
15. Drolet MC, Roussel E, Deshaies Y, Couet J, Arsenault M. A high fat/high carbohydrate diet induces aortic valve disease in C57BL/6J mice. J Am Coll Cardiol. 2006;47:850-855.
16. Duerbeck NB, Dowling DD. Vitamin A: too much of a good thing? Obstet Gynecol Surv. 2012;67:122-128.
17. Theodosiou M, Laudet V, Schubert M. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cell Mol Life Sci. 2010;67:1423-1445.
18. Rochette-Egly C, Germain P. Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl Recept Signal. 2009;7:e005.
19. Ziouzenkova O, Plutzky J. Retinoid metabolism and nuclear receptor responses: New insights into coordinated regulation of the PPAR-RXR complex. FEBS Lett. 2008;582:32-38.
20. Vermot J, Niederreither K, Garnier JM, Chambon P, Dollé P. Decreased embryonic retinoic acid synthesis results in a DiGeorge syndrome phe-notype in newborn mice. Proc Natl Acad Sci USA. 2003;100:1763-1768.
21. Ryckebüsch L, Bertrand N, Mesbah K, Bajolle F, Niederreither K, Kelly RG, Zaffran S. Decreased levels of embryonic retinoic acid synthesis accelerate recovery from arterial growth delay in a mouse model of DiGeorge syndrome. Circ Res. 2010;106:686-694.
22. Sakabe M, Kokubo H, Nakajima Y, Saga Y. Ectopic retinoic acid signaling affects outfow tract cushion development through suppression of the myocardial Tbx2-Tgfβ2 pathway. Development. 2012;139:385-395.
23. Gruber PJ, Kubalak SW, Pexieder T, Sucov HM, Evans RM, Chien KR. RXR alpha defciency confers genetic susceptibility for aortic sac, conotruncal, atrioventricular cushion, and ventricular muscle defects in mice. J Clin Invest. 1996;98:1332-1343.
24. Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR, Evans RM. RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 1994;8:1007-1018.
25. Pavan M, Ruiz VF, Silva FA, Sobreira TJ, Cravo RM, Vasconcelos M, Marques LP, Mesquita SM, Krieger JE, Lopes AA, Oliveira PS, Pereira AC, Xavier-Neto J. ALDH1A2 (RALDH2) genetic variation in human congenital heart disease. BMC Med Genet. 2009;10:113.
26. Ryckebusch L, Wang Z, Bertrand N, Lin SC, Chi X, Schwartz R, Zaffran S, Niederreither K. Retinoic acid defciency alters second heart feld formation. Proc Natl Acad Sci USA. 2008;105:2913-2918.
27. Jiang X, Choudhary B, Merki E, Chien KR, Maxson RE, Sucov HM. Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mech Dev. 2002;117:115-122.
28. Keyte A, Hutson MR. The neural crest in cardiac congenital anomalies. Differentiation. 2012;84:25-40.
29. Brade T, Kumar S, Cunningham TJ, Chatzi C, Zhao X, Cavallero S, Li P, Sucov HM, Ruiz-Lozano P, Duester G. Retinoic acid stimulates myo-cardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2. Development. 2011;138:139-148.
30. Tran CM, Sucov HM. The RXRalpha gene functions in a non-cell-autonomous manner during mouse cardiac morphogenesis. Development. 1998;125:1951-1956.
31. Lin SC, Dollé P, Ryckebüsch L, Noseda M, Zaffran S, Schneider MD, Niederreither K. Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc Natl Acad Sci USA. 2010;107:9234-9239.
32. Sorrell MR, Waxman JS. Restraint of Fgf8 signaling by retinoic acid signaling is required for proper heart and forelimb formation. Dev Biol. 2011;358:44-55.
33. Pérez-Pomares JM, Phelps A, Sedmerova M, Carmona R, González-Iriarte M, Muñoz-Chápuli R, Wessels A. Experimental studies on the spatiotem-poral expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev Biol. 2002;247:307-326.
34. von Gise A, Zhou B, Honor LB, Ma Q, Petryk A, Pu WT. WT1 regulates epicardial epithelial to mesenchymal transition through β-catenin and retinoic acid signaling pathways. Dev Biol. 2011;356:421-431.
35. Braitsch CM, Combs MD, Quaggin SE, Yutzey KE. Pod1/Tcf21 is regulated by retinoic acid signaling and inhibits differentiation of epi-cardium-derived cells into smooth muscle in the developing heart. Dev Biol. 2012;368:345-357.
36. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, Dollé P. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development. 2001;128:1019-1031.
37. Peacock JD, Levay AK, Gillaspie DB, Tao G, Lincoln J. Reduced sox9 function promotes heart valve calcifcation phenotypes in vivo. Circ Res. 2010;106:712-719.
38. Lincoln J, Lange AW, Yutzey KE. Hearts and bones: shared regulatory mechanisms in heart valve, cartilage, tendon, and bone development. Dev Biol. 2006;294:292-302.
39. Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PP, Cheah KS, Koopman P. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chon-drogenesis in the mouse. Dev Biol. 1997;183:108-121.
40. Levay AK, Peacock JD, Lu Y, Koch M, Hinton RB Jr, Kadler KE, Lincoln J. Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res. 2008;103:948-956.
41. Schuster GU, Kenyon NJ, Stephensen CB. Vitamin A defciency decreases and high dietary vitamin A increases disease severity in the mouse model of asthma. J Immunol. 2008;180:1834-1842.
42. Sagazio A, Piantedosi R, Alba M, Blaner WS, Salvatori R. Vitamin A defciency does not infuence longitudinal growth in mice. Nutrition. 2007;23:483-488.
43. Kitaoka K, Hattori A, Chikahisa S, Miyamoto K, Nakaya Y, Sei H. Vitamin A defciency induces a decrease in EEG delta power during sleep in mice. Brain Res. 2007;1150:121-130.
44. Kuwata T, Wang IM, Tamura T, Ponnamperuma RM, Levine R, Holmes KL, Morse HC, De Luca LM, Ozato K. Vitamin A def-ciency in mice causes a systemic expansion of myeloid cells. Blood. 2000;95:3349-3356.
45. Aggarwal S, Kim SW, Cheon K, Tabassam FH, Yoon JH, Koo JS. Nonclassical action of retinoic acid on the activation of the cAMP response element-binding protein in normal human bronchial epithelial cells. Mol Biol Cell. 2006;17:566-575.
46. 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.
47. Umemiya H, Fukasawa H, Ebisawa M, Eyrolles L, Kawachi E, Eisenmann G, Gronemeyer H, Hashimoto Y, Shudo K, Kagechika H. Regulation of retinoidal actions by diazepinylbenzoic acids. Retinoid synergists which activate the RXR-RAR heterodimers. J Med Chem. 1997;40:4222-4234.
48. Peacock JD, Huk DJ, Ediriweera HN, Lincoln J. Sox9 transcriptionally represses Spp1 to prevent matrix mineralization in maturing heart valves and chondrocytes. PLoS ONE. 2011;6:e26769.
49. Omenn GS, Goodman GE, Thornquist MD, Balmes J, Cullen MR, Glass A, Keogh JP, Meyskens FL, Valanis B, Williams JH, Barnhart S, Hammar S. Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med. 1996;334:1150-1155.
50. Rapola JM, Virtamo J, Ripatti S, Huttunen JK, Albanes D, Taylor PR, Heinonen OP. Randomised trial of alpha-tocopherol and beta-carotene supplements on incidence of major coronary events in men with previous myocardial infarction. Lancet. 1997;349:1715-1720.
51. Street DA, Comstock GW, Salkeld RM, Schüep W, Klag MJ. Serum antioxidants and myocardial infarction. Are low levels of carotenoids and alpha-tocopherol risk factors for myocardial infarction? Circulation. 1994;90:1154-1161.
52. Hennekens CH, Buring JE, Manson JE, Stampfer M, Rosner B, Cook NR, Belanger C, LaMotte F, Gaziano JM, Ridker PM, Willett W, Peto R. Lack of effect of long-term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. N Engl J Med. 1996;334:1145-1149.
53. Lee IM, Cook NR, Manson JE, Buring JE, Hennekens CH. Beta-carotene supplementation and incidence of cancer and cardiovascular disease: the Women's Health Study. J Natl Cancer Inst. 1999;91:2102-2106.
54. Takeda N, Manabe I, Shindo T, Iwata H, Iimuro S, Kagechika H, Shudo K, Nagai R. Synthetic retinoid Am80 reduces scavenger receptor expression and atherosclerosis in mice by inhibiting IL-6. Arterioscler Thromb Vasc Biol. 2006;26:1177-1183.
55. Harari A, Harats D, Marko D, Cohen H, Barshack I, Kamari Y, Gonen A, Gerber Y, Ben-Amotz A, Shaish A. A 9-cis beta-carotene-enriched diet inhibits atherogenesis and fatty liver formation in LDL receptor knockout mice. J Nutr. 2008;138:1923-1930.
56. Strebel RF, Girerd RJ, Wagner BM. Cardiovascular calcifcation in rats with hypervitaminosis A. Arch Pathol. 1969;87:290-297.
57. Jacobson A, Johansson S, Branting M, Melhus H. Vitamin A differentially regulates RANKL and OPG expression in human osteoblasts. Biochem Biophys Res Commun. 2004;322:162-167.
58. Roberts SJ, Chen Y, Moesen M, Schrooten J, Luyten FP. Enhancement of osteogenic gene expression for the differentiation of human periosteal derived cells. Stem Cell Res. 2011;7:137-144.
59. Luther G, Wagner ER, Zhu G, et al. BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential. Curr Gene Ther. 2011;11:229-240.
60. Weston AD, Chandraratna RA, Torchia J, Underhill TM. Requirement for RAR-mediated gene repression in skeletal progenitor differentiation. J Cell Biol. 2002;158:39-51.
61. Rhee EJ, Nallamshetty S, Plutzky J. Retinoid metabolism and its effects on the vasculature. Biochim Biophys Acta. 2012;1821:230-240.
62. Kawakami Y, Tsuda M, Takahashi S, Taniguchi N, Esteban CR, Zemmyo M, Furumatsu T, Lotz M, Izpisúa Belmonte JC, Asahara H. Transcriptional coactivator PGC-1alpha regulates chondrogenesis via association with Sox9. Proc Natl Acad Sci USA. 2005;102:2414-2419.
63. Semba I, Nonaka K, Takahashi I, Takahashi K, Dashner R, Shum L, Nuckolls GH, Slavkin HC. Positionally-dependent chondrogen-esis induced by BMP4 is co-regulated by Sox9 and Msx2. Dev Dyn. 2000;217:401-414.
64. Furumatsu T, Tsuda M, Yoshida K, Taniguchi N, Ito T, Hashimoto M, Ito T, Asahara H. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J Biol Chem. 2005;280:35203-35208.
65. Rau MJ, Fischer S, Neumann CJ. Zebrafsh Trap230/Med12 is required as a coactivator for Sox9-dependent neural crest, cartilage and ear development. Dev Biol. 2006;296:83-93.
66. Schmidt RJ, Tancredi DJ, Ozonoff S, Hansen RL, Hartiala J, Allayee H, Schmidt LC, Tassone F, Hertz-Picciotto I. Maternal periconceptional folic acid intake and risk of autism spectrum disorders and developmental delay in the CHARGE (CHildhood Autism Risks from Genetics and Environment) case-control study. Am J Clin Nutr. 2012;96:80-89.
67. Wirrig EE, Hinton RB, Yutzey KE. Differential expression of cartilage and bone-related proteins in pediatric and adult diseased aortic valves. J Mol Cell Cardiol. 2011;50:561-569.
68. Yang X, Meng X, Su X, Mauchley DC, Ao L, Cleveland JC Jr, Fullerton DA. Bone morphogenic protein 2 induces Runx2 and osteopontin expression in human aortic valve interstitial cells: role of Smad1 and extracellular signal-regulated kinase. J Thorac Cardiovasc Surg. 2009;138:1008-1015.
69. Rajamannan NM. The role of Lrp5/6 in cardiac valve disease: experimental hypercholesterolemia in the ApoE-/-/Lrp5-/-mice. J Cell Biochem. 2011;112:2987-2991.
70. Rajamannan NM, Subramaniam M, Caira F, Stock SR, Spelsberg TC. Atorvastatin inhibits hypercholesterolemia-induced calcifcation in the aortic valves via the Lrp5 receptor pathway. Circulation. 2005;112(suppl 9):I229-I234.
71. Lincoln J, Kist R, Scherer G, Yutzey KE. Sox9 is required for precursor cell expansion and extracellular matrix organization during mouse heart valve development. Dev Biol. 2007;305:120-132.
72. Wirrig EE, Yutzey KE. Transcriptional regulation of heart valve development and disease. Cardiovasc Pathol. 2011;20:162-167.
73. Beazley KE, Deasey S, Lima F, Nurminskaya MV. Transglutaminase 2-mediated activation of β-catenin signaling has a critical role in warfarin-induced vascular calcifcation. Arterioscler Thromb Vasc Biol. 2012;32:123-130.
74. Alferi CM, Cheek J, Chakraborty S, Yutzey KE. Wnt signaling in heart valve development and osteogenic gene induction. Dev Biol. 2010;338:127-135.