Issue
Modulation of S100 and smooth muscle actin-α immunoreactivity in the wall of aorta after vitamin D administration in rats with high fat diet
Corresponding Author(s) : Hala Elwy Hashem
Cellular and Molecular Biology,
Vol. 64 No. 4: Issue 4
Abstract
High fat diet is a risk factor for the development of atherosclerosis. Hence, research studies are important to understand the cellular and molecular mechanisms of atherosclerosis pathogenesis. The current study was conducted to evaluate the role of vitamin D in modulation of aortic histopathological, immunohistochemical alterations and biochemical changes induced by high fat diet in male albino rats. Forty adult rats were divided into three major groups; group I (control), group II (High fat diet) and group III (High fat diet with vitamin D). At the end of the experiment, blood cholesterol and triglycerides were determined. Aortic arches specimens were collected for histopathological study and immunohistochemical staining. Aorta of high fat diet group showed intimal thickening with vacuolated endothelial cells. The tunica media showed areas of fibrosis and irregular vacuolated smooth muscle cells. Many inflammatory cells were detected in the tunica adventitia. Significant reduction in area percentage of smooth muscle actin-α (SMA-α) immunoreactivity and increase in number of S100 positive dendritic cells (DCs) with significant increase in serum cholesterol and triglycerides were also detected. Concomitant vitamin D supplementation, with high fat diet, showed amelioration in histopathological aortic changes with significant increase in SMA-α immunoreactivity and decrease in S100 positive (DCs). However, serum cholesterol and triglyceride showed non-significant decrease after vitamin D supplementation. In conclusion, vitamin D administration ameliorates aortic wall histoopathological changes induced by high fat diet most probably through local modulation of S100 and SMA-α immunoreactivity. Hence, vitamin D could be suggested as a protective agent against aortic atherosclerotic changes.
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- WHO. World Health Organization Statistical Information System (WHOSIS). Geneva, Switzerland; 2010.
- Swirski FK, Pittet, MJ, Kircher MF. Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci U S A 2006; 103: 10340–10345.
- Profumo E, Buttari B, Saso L, Capoano R, Salvati B, Rigano R. T lymphocyte autoreactivity in inflammatory mechanisms regulating atherosclerosis. Sci World J 2012; 157534, 9 pages.
- Woollard KJ. Immunological aspects of atherosclerosis. Clin Sci 2013; 125: 221–235.
- Doran AC, Meller N, McNamara CA. Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol 2008; 28: 812–819.
- Rossi M and Young JW. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J Immunol 2005; 175: 1373–1381.
- Shortman K and Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007; 7: 19–30.
- Choi JH, Do Y, Cheong C, Koh H, Boscardin SB, Oh YS et al. Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J Exp Med 2009; 206: 497–505.
- Van Vré EA, Hoymans VY, Bult H, Lenjou M, Van Bockstaele DR, Vrints CJ et al. Decreased number of circulating plasmacytoid dendritic cells in patients with atherosclerotic coronary artery disease. Coron Artery Dis 2006; 17: 243–248.
- Van Vré EA, Van Brussel I, Bosmans JM, Vrints CJ, Bult H. Dendritic cells in human atherosclerosis: from circulation to atherosclerotic plaques. Mediators Inflamm 2011: 941396, 2011; 13 pages. http://dx.doi.org/10.1155/2011/941396.
- Van Vré EA, Van Brussel I, deBeeck KO, Hoymans VY, Vrints CJ, Bult H et al. Changes in blood dendritic cell counts in relation to type of coronary artery disease and brachial endothelial cell function. Coron Artery Dis 2010; 21: 87–96.
- Seong SY and Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004; 4: 469–478.
- Institute of Medicine. Food and Nutrition Board. Dietary Reference Intakes for Calcium and Vitamin D. Washington, DC: Nat Acad Press (US); 2010.
- Temmerman JC. Vitamin D and Cardiovascular Disease. J Am Coll Nutr 2011; 30: 167-170.
- Carrelli AL, Walker MD, Lowe H, McMahon DJ, Rundek T, Sacco RL et al. Vitamin D deficiency is associated with subclinical carotid atherosclerosis. Stroke 2011; 42: 2240-2245.
- Oz F, Cizgici AY, Oflaz H. Impact of vitamin D insufficiency on the epicardial coronary flow velocity and endothelial function. Coron Artery Dis 2013; 24: 392–397.
- Lupoli R, Vaccaro A, Ambrosino P, Poggio P, Amato M, Minno MD. Impact of Vitamin D Deficiency on Subclinical Carotid Atherosclerosis: A Pooled Analysis of Cohort Studies. J Clinical Endocrinol Metab 2017; 102: 2146–2153
- Riek AE, Oh J, Sprague JE, Timpson A, de las Fuentes L, Bernal-Mizrachi L et al. Vitamin D suppression of endoplasmic reticulum stress promotes an antiatherogenic monocyte/macrophage phenotype in type 2 diabetic patients. J Biol Chem 2012; 287: 38482–38494.
- Riek AE, Oh J, Bernal-Mizrachi C. 1,25(OH)2 vitamin D suppresses macrophage migration and reverses atherogenic cholesterol metabolism in type 2 diabetic patients. J Steroid Biochem Molecular Biol 2013; 136: 309–312.
- Takeda M, Yamashita T, Sasaki N, Nakajima K, Kita T, Shinohara M et al. Oral administration of an active form of vitamin d3 (calcitriol) decreases atherosclerosis in mice by inducing regulatory T cells and immature dendritic cells with tolerogenic functions. Arterioscl Thromb Vasc Biol 2010; 30: 2495-2503.
- Bobryshev YV. Vitamin D3 suppresses immune reactions in atherosclerosis, affecting regulatory T cells and dendritic cell function. Arterioscl Thromb Vasc Biol 2010; 30: 2317-2319.
- Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Cin ED et al. Vitamin D3 Affects Differentiation, Maturation, and Function of Human Monocyte-Derived Dendritic Cells. J Immunol 2000; 164: 4443-4451.
- Mangge H, Weghuber D, Prassl R, Haara A, Schnedl W, Postolache TT et al. The Role of Vitamin D in Atherosclerosis Inflammation Revisited: More a Bystander than a Player? Curr Vasc Pharmacol 2015; 13: 392-398.
- Institute of Laboratory animals Resources, Commission on Life Science, National Research Council. Guide for the Care and Use of Labomouseory Animals. National Academy Press, Washington D.C., 1996, p.21-55.
- Chabas JF, Stephan D, Marqueste T, Garcia S, Lavaut MN, Nguyen C et al. Cholecalciferol (Vitamin D3) Improves Myelination and Recovery after Nerve Injury. Plos One 2013; 8: e65034. doi:10.1371/journal.pone.0065034.
- Thirumalai T, Tamilselvan N, David E. Hypolipidemic activity of Piper betel in high fat diet induced hyperlipidemic rat. J Acute Disease 2014; 2: 131-135.
- Altunkaynak Z. Effects of high fat diet induced obesity on female rat livers (a histochemical study). Eur J Gen Med 2005; 2: 100-109.
- Park CY, Lee WH, Fleet JC, Allen MR, McCabe GP, Walsh DM et al. Calcium and vitamin D intake maintained from preovariectomy independently affect calcium metabolism and bone properties in Sprague Dawley rats. Osteoporos Int 2014; 25: 1905–1915.
- Novelli EL, Diniz YS, Galhardi CM, Ebaid GM, Rodrigues HG, Mani F et al. Anthropometrical parameters and markers of obesity in rats. Lab Anim 2007; 41:111-119.
- Bancroft JD and Gamble M. Theory and practice of histological techniques. 6th ed. Scotland, London: Churchill Livingstone, London; 2008, p. 125-138.
- Kiernan JA. Histological and Histochemical methods: Theory and practice. Butterworth-Heinemann, Oxford; 1999.
- Fang Z, Deng Q, Hu H, Wang X, Sun X, Ge X et al. Characteristics of immunogenic and tolerogenic dendritic cells within the arterial wall in atherosclerosis and in vitro. Int J Clin Exp Med 2014; 7: 4846–4856.
- Matsumoto S, Gotoh N, Hishinuma S, Abe Y, Shimizu Y, Katano Y et al. Atherosclerosis and endothelial dysfunction. Nutrients 2014; 6: 1236-1250.
- Menezes AR Lamb MC, Lavie CJ, Di Nicolantonio JJ. Vitamin D and atherosclerosis. Curr Opin Cardiol 2014; 29: 571-577.
- Rudijanto A. The role of vascular smooth muscle cells on the pathogenesis of atherosclerosis. Acta Med Indones 2007; 39: 86-93.
- Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN et al. Triglycerides and Cardiovascular Disease. Circulation 2011; 123: 2292–2333.
- Teno S, Uto Y, Nagashima H, Endoh Y, Iwamoto Y, Onmori Y et al. Association of postprandial hypertriglyceridemia and carotid intima-media thickness in patients with type 2 diabetes. Diabetes Care 2000; 23:1401–1406.
- Lavie CJ, Dinicolantonio JJ, Milani RV. Vitamin D and cardiovascular health. Circulation 2013; 128: 2404–2406.
- Griendhing KK and Alexander RW. Oxidative stress and cardiovascular disease. Circulation 1997; 96: 3264-3265.
- Subbotin VM. Neovascularization of coronary tunica intima (DIT) is the cause of coronary atherosclerosis. Lipoproteins invade coronary intima via neovascularization from adventitial vasa vasorum, but not from the arterial lumen: a hypothesis. Theor Biol Med Model 2012; 9: 11-33.
- Ali MM, Sarasa A, Bharati A. Effect of crude extract of Bombyx mori coccoons in hyperlipidemia and atherosclerosis. J Ayurveda Integrative Med 2011; 2: 72-78.
- Chen X, Huang Z, Ran W, Liao G, Zha L, Wang Z. Type 2 diabetes mellitus control and atherosclerosis prevention in a non obese rat model using duodenal jejunal bypass. Experiment Therap Med 2014; 8: 856-862.
- Komolafe OA, Ofusori DA, Adewole OS, Ayoka AO, Bejide R. Histological and histochemical studies of the aorta and pulmonary trunk in STZ-induced diabetic wistar rats treated with Momordica Charantia. Int J Morphol 2013; 31: 716-723.
- Hansson GK and Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006; 6: 508-519.
- Liu JX, Xiang J, Bu RF, Wu WJ, Shen H, Wang XJ. Serum 25-hydroxyvitamin D concentration is negatively related to carotid artery intima-media thickness in type 2 diabetic patients. Zhonghua Xin Xue Guan Bing Za Zhi 2012; 40: 115–119 (abstract).
- Uberti F, Lattuada D, Morsanuto V, Nava U, Bolis G, Vacca G et al. Vitamin D Protects Human Endothelial Cells From Oxidative Stress Through the Autophagic and Survival Pathways. J Clin Endocrinol Metab 2014; 99: 1367–1374.
- Andrukhova O, Slavic S, Zeitz U. Vitamin D is a regulator of endothelial nitric oxide synthase and arterial stiffness in mice. Mol Endocrinol 2014; 28: 53–64.
- Chen S, Law CS, Gardner DG. Vitamin D-dependent suppression of endothelin-induced vascular smooth muscle cell proliferation through inhibition of CDK2 activity. J Steroid Biochem Mol Biol 2010; 118: 135–141.
- Somjen D, Weisman Y, Kohen F. 25-hydroxyvitamin D3-1alpha-hydroxylase is expressed in human vascular smooth muscle cells and is upregulated by parathyroid hormone and estrogenic compounds. Circulation 2005; 111: 1666–1671.
- Kasuga H, Hosogane N, Matsuoka K, Mori I, Sakura Y, Shimakawa K et al. Characterization of transgenic rats constitutively expressing vitamin D-24-hydroxylase gene. Biochem. Biophys Res Commun 2002; 297: 1332-1338.
- Norman PE and Powell JT. Vitamin D and cardiovascular disease. Circulation Research 2014; 114, 379–393.
- Andersen R, Brot C, Mejborn H, Mí¸lgaard C, Skovgaard LT, Trolle E et al. Vitamin D supplementation does not affect serum lipids and lipoproteins in Pakistani immigrants. Eur J Clin Nutr 2009; 63: 1150-1153.
- Wang H, Xia N, Yang Y, Peng DQ. Influence of vitamin D supplementation on plasma lipid profiles: A meta-analysis of randomized controlled trials. Lipids Health Dis 2012; 11: 42.
- Vanlint S. Vitamin D and Obesity. Nutrients 2013; 5: 949-956.
- Choi SK, Park JA, Ham SK, Yoon JY, Kim SM, Kim JY et al. Association between vitamin D and serum cholesterol. Korean J Fam Pract 2015; 5: 441-446.
- Rodríguez-Rodríguez E, Ortega RM, González-Rodríguez LG, López-Sobaler AM. Vitamin D deficiency is an independent predictor of elevated triglycerides in Spanish school children. Eur J Nutr 2011; 50: 373-378.
- Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler Thromb Vasc Biol 1999; 19: 1589-94.
- Haddad Y, Lahoute C, Clément M, Laurans L, Metghalchi S, Zeboudj L et al. The Dendritic Cell Receptor DNGR-1 Promotes the Development of Atherosclerosis in Mice. Circ Res 2017; 121: 234-243.
- Lin W, Wang W, Wang D, Ling W. Quercetin protects against atherosclerosis by inhibiting dendritic cell activation. Mol Nutr Food Res 2017; 61: 1700031.
References
WHO. World Health Organization Statistical Information System (WHOSIS). Geneva, Switzerland; 2010.
Swirski FK, Pittet, MJ, Kircher MF. Monocyte accumulation in mouse atherogenesis is progressive and proportional to extent of disease. Proc Natl Acad Sci U S A 2006; 103: 10340–10345.
Profumo E, Buttari B, Saso L, Capoano R, Salvati B, Rigano R. T lymphocyte autoreactivity in inflammatory mechanisms regulating atherosclerosis. Sci World J 2012; 157534, 9 pages.
Woollard KJ. Immunological aspects of atherosclerosis. Clin Sci 2013; 125: 221–235.
Doran AC, Meller N, McNamara CA. Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol 2008; 28: 812–819.
Rossi M and Young JW. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J Immunol 2005; 175: 1373–1381.
Shortman K and Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 2007; 7: 19–30.
Choi JH, Do Y, Cheong C, Koh H, Boscardin SB, Oh YS et al. Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J Exp Med 2009; 206: 497–505.
Van Vré EA, Hoymans VY, Bult H, Lenjou M, Van Bockstaele DR, Vrints CJ et al. Decreased number of circulating plasmacytoid dendritic cells in patients with atherosclerotic coronary artery disease. Coron Artery Dis 2006; 17: 243–248.
Van Vré EA, Van Brussel I, Bosmans JM, Vrints CJ, Bult H. Dendritic cells in human atherosclerosis: from circulation to atherosclerotic plaques. Mediators Inflamm 2011: 941396, 2011; 13 pages. http://dx.doi.org/10.1155/2011/941396.
Van Vré EA, Van Brussel I, deBeeck KO, Hoymans VY, Vrints CJ, Bult H et al. Changes in blood dendritic cell counts in relation to type of coronary artery disease and brachial endothelial cell function. Coron Artery Dis 2010; 21: 87–96.
Seong SY and Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004; 4: 469–478.
Institute of Medicine. Food and Nutrition Board. Dietary Reference Intakes for Calcium and Vitamin D. Washington, DC: Nat Acad Press (US); 2010.
Temmerman JC. Vitamin D and Cardiovascular Disease. J Am Coll Nutr 2011; 30: 167-170.
Carrelli AL, Walker MD, Lowe H, McMahon DJ, Rundek T, Sacco RL et al. Vitamin D deficiency is associated with subclinical carotid atherosclerosis. Stroke 2011; 42: 2240-2245.
Oz F, Cizgici AY, Oflaz H. Impact of vitamin D insufficiency on the epicardial coronary flow velocity and endothelial function. Coron Artery Dis 2013; 24: 392–397.
Lupoli R, Vaccaro A, Ambrosino P, Poggio P, Amato M, Minno MD. Impact of Vitamin D Deficiency on Subclinical Carotid Atherosclerosis: A Pooled Analysis of Cohort Studies. J Clinical Endocrinol Metab 2017; 102: 2146–2153
Riek AE, Oh J, Sprague JE, Timpson A, de las Fuentes L, Bernal-Mizrachi L et al. Vitamin D suppression of endoplasmic reticulum stress promotes an antiatherogenic monocyte/macrophage phenotype in type 2 diabetic patients. J Biol Chem 2012; 287: 38482–38494.
Riek AE, Oh J, Bernal-Mizrachi C. 1,25(OH)2 vitamin D suppresses macrophage migration and reverses atherogenic cholesterol metabolism in type 2 diabetic patients. J Steroid Biochem Molecular Biol 2013; 136: 309–312.
Takeda M, Yamashita T, Sasaki N, Nakajima K, Kita T, Shinohara M et al. Oral administration of an active form of vitamin d3 (calcitriol) decreases atherosclerosis in mice by inducing regulatory T cells and immature dendritic cells with tolerogenic functions. Arterioscl Thromb Vasc Biol 2010; 30: 2495-2503.
Bobryshev YV. Vitamin D3 suppresses immune reactions in atherosclerosis, affecting regulatory T cells and dendritic cell function. Arterioscl Thromb Vasc Biol 2010; 30: 2317-2319.
Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Cin ED et al. Vitamin D3 Affects Differentiation, Maturation, and Function of Human Monocyte-Derived Dendritic Cells. J Immunol 2000; 164: 4443-4451.
Mangge H, Weghuber D, Prassl R, Haara A, Schnedl W, Postolache TT et al. The Role of Vitamin D in Atherosclerosis Inflammation Revisited: More a Bystander than a Player? Curr Vasc Pharmacol 2015; 13: 392-398.
Institute of Laboratory animals Resources, Commission on Life Science, National Research Council. Guide for the Care and Use of Labomouseory Animals. National Academy Press, Washington D.C., 1996, p.21-55.
Chabas JF, Stephan D, Marqueste T, Garcia S, Lavaut MN, Nguyen C et al. Cholecalciferol (Vitamin D3) Improves Myelination and Recovery after Nerve Injury. Plos One 2013; 8: e65034. doi:10.1371/journal.pone.0065034.
Thirumalai T, Tamilselvan N, David E. Hypolipidemic activity of Piper betel in high fat diet induced hyperlipidemic rat. J Acute Disease 2014; 2: 131-135.
Altunkaynak Z. Effects of high fat diet induced obesity on female rat livers (a histochemical study). Eur J Gen Med 2005; 2: 100-109.
Park CY, Lee WH, Fleet JC, Allen MR, McCabe GP, Walsh DM et al. Calcium and vitamin D intake maintained from preovariectomy independently affect calcium metabolism and bone properties in Sprague Dawley rats. Osteoporos Int 2014; 25: 1905–1915.
Novelli EL, Diniz YS, Galhardi CM, Ebaid GM, Rodrigues HG, Mani F et al. Anthropometrical parameters and markers of obesity in rats. Lab Anim 2007; 41:111-119.
Bancroft JD and Gamble M. Theory and practice of histological techniques. 6th ed. Scotland, London: Churchill Livingstone, London; 2008, p. 125-138.
Kiernan JA. Histological and Histochemical methods: Theory and practice. Butterworth-Heinemann, Oxford; 1999.
Fang Z, Deng Q, Hu H, Wang X, Sun X, Ge X et al. Characteristics of immunogenic and tolerogenic dendritic cells within the arterial wall in atherosclerosis and in vitro. Int J Clin Exp Med 2014; 7: 4846–4856.
Matsumoto S, Gotoh N, Hishinuma S, Abe Y, Shimizu Y, Katano Y et al. Atherosclerosis and endothelial dysfunction. Nutrients 2014; 6: 1236-1250.
Menezes AR Lamb MC, Lavie CJ, Di Nicolantonio JJ. Vitamin D and atherosclerosis. Curr Opin Cardiol 2014; 29: 571-577.
Rudijanto A. The role of vascular smooth muscle cells on the pathogenesis of atherosclerosis. Acta Med Indones 2007; 39: 86-93.
Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN et al. Triglycerides and Cardiovascular Disease. Circulation 2011; 123: 2292–2333.
Teno S, Uto Y, Nagashima H, Endoh Y, Iwamoto Y, Onmori Y et al. Association of postprandial hypertriglyceridemia and carotid intima-media thickness in patients with type 2 diabetes. Diabetes Care 2000; 23:1401–1406.
Lavie CJ, Dinicolantonio JJ, Milani RV. Vitamin D and cardiovascular health. Circulation 2013; 128: 2404–2406.
Griendhing KK and Alexander RW. Oxidative stress and cardiovascular disease. Circulation 1997; 96: 3264-3265.
Subbotin VM. Neovascularization of coronary tunica intima (DIT) is the cause of coronary atherosclerosis. Lipoproteins invade coronary intima via neovascularization from adventitial vasa vasorum, but not from the arterial lumen: a hypothesis. Theor Biol Med Model 2012; 9: 11-33.
Ali MM, Sarasa A, Bharati A. Effect of crude extract of Bombyx mori coccoons in hyperlipidemia and atherosclerosis. J Ayurveda Integrative Med 2011; 2: 72-78.
Chen X, Huang Z, Ran W, Liao G, Zha L, Wang Z. Type 2 diabetes mellitus control and atherosclerosis prevention in a non obese rat model using duodenal jejunal bypass. Experiment Therap Med 2014; 8: 856-862.
Komolafe OA, Ofusori DA, Adewole OS, Ayoka AO, Bejide R. Histological and histochemical studies of the aorta and pulmonary trunk in STZ-induced diabetic wistar rats treated with Momordica Charantia. Int J Morphol 2013; 31: 716-723.
Hansson GK and Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006; 6: 508-519.
Liu JX, Xiang J, Bu RF, Wu WJ, Shen H, Wang XJ. Serum 25-hydroxyvitamin D concentration is negatively related to carotid artery intima-media thickness in type 2 diabetic patients. Zhonghua Xin Xue Guan Bing Za Zhi 2012; 40: 115–119 (abstract).
Uberti F, Lattuada D, Morsanuto V, Nava U, Bolis G, Vacca G et al. Vitamin D Protects Human Endothelial Cells From Oxidative Stress Through the Autophagic and Survival Pathways. J Clin Endocrinol Metab 2014; 99: 1367–1374.
Andrukhova O, Slavic S, Zeitz U. Vitamin D is a regulator of endothelial nitric oxide synthase and arterial stiffness in mice. Mol Endocrinol 2014; 28: 53–64.
Chen S, Law CS, Gardner DG. Vitamin D-dependent suppression of endothelin-induced vascular smooth muscle cell proliferation through inhibition of CDK2 activity. J Steroid Biochem Mol Biol 2010; 118: 135–141.
Somjen D, Weisman Y, Kohen F. 25-hydroxyvitamin D3-1alpha-hydroxylase is expressed in human vascular smooth muscle cells and is upregulated by parathyroid hormone and estrogenic compounds. Circulation 2005; 111: 1666–1671.
Kasuga H, Hosogane N, Matsuoka K, Mori I, Sakura Y, Shimakawa K et al. Characterization of transgenic rats constitutively expressing vitamin D-24-hydroxylase gene. Biochem. Biophys Res Commun 2002; 297: 1332-1338.
Norman PE and Powell JT. Vitamin D and cardiovascular disease. Circulation Research 2014; 114, 379–393.
Andersen R, Brot C, Mejborn H, Mí¸lgaard C, Skovgaard LT, Trolle E et al. Vitamin D supplementation does not affect serum lipids and lipoproteins in Pakistani immigrants. Eur J Clin Nutr 2009; 63: 1150-1153.
Wang H, Xia N, Yang Y, Peng DQ. Influence of vitamin D supplementation on plasma lipid profiles: A meta-analysis of randomized controlled trials. Lipids Health Dis 2012; 11: 42.
Vanlint S. Vitamin D and Obesity. Nutrients 2013; 5: 949-956.
Choi SK, Park JA, Ham SK, Yoon JY, Kim SM, Kim JY et al. Association between vitamin D and serum cholesterol. Korean J Fam Pract 2015; 5: 441-446.
Rodríguez-Rodríguez E, Ortega RM, González-Rodríguez LG, López-Sobaler AM. Vitamin D deficiency is an independent predictor of elevated triglycerides in Spanish school children. Eur J Nutr 2011; 50: 373-378.
Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler Thromb Vasc Biol 1999; 19: 1589-94.
Haddad Y, Lahoute C, Clément M, Laurans L, Metghalchi S, Zeboudj L et al. The Dendritic Cell Receptor DNGR-1 Promotes the Development of Atherosclerosis in Mice. Circ Res 2017; 121: 234-243.
Lin W, Wang W, Wang D, Ling W. Quercetin protects against atherosclerosis by inhibiting dendritic cell activation. Mol Nutr Food Res 2017; 61: 1700031.