Vitamin A-deficient diet accelerated atherogenesis in apolipoprotein E-/- mice and dietary β -carotene prevents this consequence

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Relevy, Noa Zolberg ^a,b   Harats, Dror ^a,b   Harari, Ayelet ^a   Ben Amotz, Ami ^c   Bitzur, Rafael ^a,b   Rühl, Ralph ^d   Shaish, Aviv ^a  

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c NBT Eilat   (Israel)

^d UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; BETA CAROTENE; RETINOL; CHOLESTEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; DUNALIELLA; MALE; MOUSE; NONHUMAN; RETINOL DEFICIENCY; ANIMAL; BLOOD; BODY WEIGHT; C57BL MOUSE; COMPLICATION; DEFICIENCY; DIETARY SUPPLEMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; INSULIN RESISTANCE; LIVER; METABOLISM; PATHOLOGY;

DUNALIELLA; MUS;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BETA CAROTENE; BODY WEIGHT; CHOLESTEROL; DIETARY SUPPLEMENTS; GENE EXPRESSION REGULATION; INSULIN RESISTANCE; LIVER; MALE; MICE, INBRED C57BL; VITAMIN A; VITAMIN A DEFICIENCY;

EID: 84924560211     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/758723     Document Type: Article

References (82)

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26. A. Shaish, J. George, B. Gilburd, P. Keren, H. Levkovitz, and D. Harats, "Dietary β-carotene and α-tocopherol combination does not inhibit atherogenesis in an ApoE-deficient mouse model," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 19, no. 6, pp. 1470-1475, 1999.
27. S. Ishibashi, J. Herz, N. Maeda, J. L. Goldstein, and M. S. Brown, "The two-receptor model of lipoprotein clearance: tests of the hypothesis in "knockout" mice lacking the low density lipopro-tein receptor, apolipoprotein E, or both proteins," Proceedings of the National Academy of Sciences of the United States of America, Vol. 91, no. 10, pp. 4431-4435, 1994.
28. Y. Yamamoto, R. Zolfaghari, and A. C. Ross, "Regulation of CYP26 (cytochrome P450RAI) mRNA expression and retinoic acid metabolism by retinoids and dietary vitamin A in liver of mice and rats," The FASEB Journal, Vol. 14, no. 13, pp. 2119-2127, 2000.
29. R. Stienstra, C. Duval, M. Müller, and S. Kersten, "PPARs, obesity, and inflammation," PPAR Research, Vol. 2007, Article ID 95974, 10 pages, 2007.
30. T. Kuwata, I.-M. Wang, T. Tamura et al., "Vitamin A deficiency in mice causes a systemic expansion of myeloid cells," Blood, Vol. 95, no. 11, pp. 3349-3356, 2000.
31. F. Andreola, D. F. Calvisi, G. Elizondo et al., "Reversal of liver fibrosis in aryl hydrocarbon receptor null mice by dietary vitamin A depletion," Hepatology, Vol. 39, no. 1, pp. 157-166, 2004.
32. C. B. Stephensen, S. R. Blount, T. R. Schoeb, and J. Y. Park, "Vitamin A deficiency impairs some aspects of the host response to in uenza A virus infection in BALB/c mice," Journal of Nutrition, Vol. 123, no. 5, pp. 823-833, 1993.
33. J. C. Bauernfeind, "Carotenoids as colorants and vitamin A precursors," in Technological and Nutritional Applications, H. A. Klaui, C. R. Adams, and W. L. Marusich, Eds., 1981.
34. A. Ben-Amotz, S. Mokady, and M. Avron, "The β-carotene-rich alga Dunaliella bardawil as a source of retinol in a rat diet," British Journal of Nutrition, Vol. 59, no. 3, pp. 443-449, 1988.
35. E. Reboul, "Absorption of vitamin A and carotenoids by the enterocyte: focus on transport proteins," Nutrients, Vol. 5, no. 9, pp. 3563-3581, 2013.
36. R. Blomhoff and K. Wake, "Perisinusoidal stellate cells of the liver: important roles in retinol metabolism and fibrosis," The FASEB Jour nal, Vol. 5, no. 3, pp. 271-277, 1991.
37. S. Fargion, M. Porzio, and A. L. Fracanzani, "Nonalcoholic fatty liver disease and vascular disease: state-of-the-art," World Journal of Gastroenterology, Vol. 20, pp. 13306-13324, 2014.
38. R. Kleemann, L. Verschuren, M. J. Van Erk et al., "Atherosclerosis and liver inflammation induced by increased dietary cholesterol intake: a combined transcriptomics and metabolomics analysis," Genome Biology, Vol. 8, article R200, 2007.
39. L. Gatica, S. Alvarez, N. Gomez et al., "Vitamin A deficiency induces prooxidant environment and inflammation in rat aorta," Free Radical Research, Vol. 39, no. 6, pp. 621-628, 2005.
40. D. N. D'Ambrosio, R. D. Clugston, and W. S. Blaner, "Vitamin A metabolism: an update," Nutrients, Vol. 3, no. 1, pp. 63-103, 2011.
41. G. P. Lobo, J. Amengual, H. N. Li et al., "β,β-carotene decreases peroxisome proliferator receptor γ activity and reduces lipid storage capacity of adipocytes in a β,β-carotene oxygenase 1-dependent manner," The Journal of Biological Chemistry, Vol. 285, no. 36, pp. 27891-27899, 2010.
42. E.-J. Rhee, S. Nallamshetty, and J. Plutzky, "Retinoid metabolism and its effects on the vasculature," Biochimica et Biophysica Acta, Vol. 1821, no. 1, pp. 230-240, 2012.
43. D. I. Axel, A. Frigge, J. Dittmann et al., "All-trans retinoic acid regulates proliferation, migration, differentiation, and extracellular matrix turnover of human arterial smooth muscle cells," Cardiovascular Research, Vol. 49, no. 4, pp. 851-862, 2001.
44. B. Zhou, Y. Pan, Z. Hu et al., "All-trans-retinoic acid ameliorated high fat diet-induced atherosclerosis in rabbits by inhibiting platelet activation and inflammation," Journal of Biomedicine and Biotechnology, Vol. 2012, Article ID 259693, 9 pages, 2012.
45. T. Langmann, G. Liebisch, C. Moehle et al., "Gene expression profiling identifies retinoids as potent inducers of macrophage lipid efflux," Biochimica et Biophysica Acta: Molecular Basis of Disease, Vol. 1740, no. 2, pp. 155-161, 2005.
46. A. Harari, R. Abecassis, N. Relevi et al., "Prevention of atherosclerosis progression by 9-cis-β-carotene rich alga Dunaliella in apoE-deficient mice," BioMed Research International, Vol. 2013, Article ID 169517, 7 pages, 2013.
47. A. Harari, D. Harats, D. Marko et al., "A 9-cis β-carotene-enriched diet inhibits atherogenesis and fatty liver formation in LDL receptor knockout mice," The Journal of Nutrition, Vol. 138, no. 10, pp. 1923-1930, 2008.
48. T. Grune, G. Lietz, A. Palou et al., "β-carotene is an important vitamin A source for humans," The Journal of Nutrition, Vol. 140, no. 12, pp. 2268S-2285S, 2010.
49. S. A. Ross, P. J. McCaffery, U. C. Drager, and L. M. de Luca, "Retinoids in embryonal development," Physiological Reviews, Vol. 80, no. 3, pp. 1021-1054, 2000.
50. J. H. Humphrey, K. P. West Jr., and A. Sommer, "Vitamin A deficiency and attributable mortality among under-5-year-olds," Bulletin of the World Health Organization, Vol. 70, pp. 225-232, 1992.
51. A. Bousvaros, D. Zurakowski, C. Duggan et al., "Vitamins A and E serum levels in children and young adults with inflammatory bowel disease: effect of disease activity," Journal of Pediatric Gastroenterology and Nutrition, Vol. 26, no. 2, pp. 129-135, 1998.
52. M. A. Leo and C. S. Lieber, "Hepatic vitamin A depletion in alcoholic liver injury," The New England Journal of Medicine, Vol. 307, no. 10, pp. 597-601, 1982.
53. A. Lindqvist, J. Sharvill, D. E. Sharvill, and S. Andersson, "Loss-of-function mutation in carotenoid 15,15'-monooxygenase identified in a patient with hypercarotenemia and hypovita-minosis A," The Journal of Nutrition, Vol. 137, no. 11, pp. 2346-2350, 2007.
54. M. C. Sales, A. de Azevedo Paiva, D. de Queiroz, R. A. F. Costa, M. A. L. da Cunha, and D. F. Pedraza, "Nutritional status of iron in children from 6 to 59 months of age and its relation to vitamin A deficiency," Nutricion Hospitalaria, Vol. 28, no. 3, pp. 734-740, 2013.
55. D. W. Goodman, H. S. Huang, and T. Shiratori, "Tissue distribution and metabolism of newly absorbed vitamin a in the rat," The Journal of Lipid Research, Vol. 6, pp. 390-396, 1965.
56. M. Kanai, A. Raz, and D. S. Goodman, "Retinol-binding protein: the transport protein for vitamin A in human plasma," The Journal of Clinical Investigation, Vol. 47, no. 9, pp. 2025-2044, 1968.
57. S. B. Kurlandsky, M. V. Gamble, R. Ramakrishnan, and W. S. Blaner, "Plasma delivery of retinoic acid to tissues in the rat," The Journal of Biological Chemistry, Vol. 270, no. 30, pp. 17850-17857, 1995.
58. H. K. Biesalski, J. Frank, S. C. Beck et al., "Biochemical but not clinical, vitamin A deficiency results from mutations in the gene for retinol binding protein," The American Journal of Clinical Nutrition, Vol. 69, no. 5, pp. 931-936, 1999.
59. L. Quadro, W. S. Blaner, D. J. Salchow et al., "Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein," The EMBO Journal, Vol. 18, no. 17, pp. 4633-4644, 1999.
60. L. V. Gatica, V. A. Vega, F. Zirulnik, L. B. Oliveros, and M. S. Gimenez, "Alterations in the lipid metabolism of rat aorta: effects of vitamin A deficiency," Journal of Vascular Research, Vol. 43, no. 6, pp. 602-610, 2006.
61. L. B. Oliveros, M. A. Domeniconi, V. A. Vega, L. V. Gatica, A. M. Brigada, and M. S. Gimenez, "Vitamin A deficiency modifies lipid metabolism in rat liver," British Journal of Nutrition, Vol. 97, no. 2, pp. 263-272, 2007.
62. S. Hessel, A. Eichinger, A. Isken et al., "CMO1 deficiency abolishes vitamin a production from β-carotene and alters lipid metabolism in mice," The Journal of Biological Chemistry, Vol. 282, no. 46, pp. 33553-33561, 2007.
63. A. Ben-Amotz, A. Lers, and M. Avron, "Stereoisomers of beta-carotene and phytoene in the alga Dunaliella bardawil," Plant Physiology, Vol. 86, no. 4, pp. 1286-1291, 1988.
64. A. Shaish, A. Daugherty, F. O'Sullivan, G. Schonfeld, and J. W. Heinecke, "Beta-carotene inhibits atherosclerosis in hyperc-holesterolemic rabbits," The Journal of Clinical Investigation, Vol. 96, no. 4, pp. 2075-2082, 1995.
65. R. Rühl, "Method to determine 4-oxo-retinoic acids, retinoic acids and retinol in serum and cell extracts by liquid chromatography/diode-array detection atmospheric pressure chemical ionisation tandem mass spectrometry," Rapid Communications in Mass Spectrometry, Vol. 20, no. 16, pp. 2497-2504, 2006.
66. S. L. Friedman and F. J. Roll, "Isolation and culture of hepatic lipocytes, Kupffer cells, and sinusoidal endothelial cells by density gradient centrifugation with Stractan," Analytical Biochemistry, Vol. 161, no. 1, pp. 207-218, 1987.
67. A. Shaish, J. George, B. Gilburd, P. Keren, H. Levkovitz, and D. Harats, "Dietary β-carotene and α-tocopherol combination does not inhibit atherogenesis in an ApoE-deficient mouse model," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 19, no. 6, pp. 1470-1475, 1999.
68. S. Ishibashi, J. Herz, N. Maeda, J. L. Goldstein, and M. S. Brown, "The two-receptor model of lipoprotein clearance: tests of the hypothesis in "knockout" mice lacking the low density lipopro-tein receptor, apolipoprotein E, or both proteins," Proceedings of the National Academy of Sciences of the United States of America, Vol. 91, no. 10, pp. 4431-4435, 1994.
69. Y. Yamamoto, R. Zolfaghari, and A. C. Ross, "Regulation of CYP26 (cytochrome P450RAI) mRNA expression and retinoic acid metabolism by retinoids and dietary vitamin A in liver of mice and rats," The FASEB Journal, Vol. 14, no. 13, pp. 2119-2127, 2000.
70. R. Stienstra, C. Duval, M. Müller, and S. Kersten, "PPARs, obesity, and inflammation," PPAR Research, Vol. 2007, Article ID 95974, 10 pages, 2007.
71. T. Kuwata, I.-M. Wang, T. Tamura et al., "Vitamin A deficiency in mice causes a systemic expansion of myeloid cells," Blood, Vol. 95, no. 11, pp. 3349-3356, 2000.
72. F. Andreola, D. F. Calvisi, G. Elizondo et al., "Reversal of liver fibrosis in aryl hydrocarbon receptor null mice by dietary vitamin A depletion," Hepatology, Vol. 39, no. 1, pp. 157-166, 2004.
73. C. B. Stephensen, S. R. Blount, T. R. Schoeb, and J. Y. Park, "Vitamin A deficiency impairs some aspects of the host response to in uenza A virus infection in BALB/c mice," Journal of Nutrition, Vol. 123, no. 5, pp. 823-833, 1993.
74. J. C. Bauernfeind, "Carotenoids as colorants and vitamin A precursors," in Technological and Nutritional Applications, H. A. Klaui, C. R. Adams, and W. L. Marusich, Eds., 1981.
75. A. Ben-Amotz, S. Mokady, and M. Avron, "The β-carotene-rich alga Dunaliella bardawil as a source of retinol in a rat diet," British Journal of Nutrition, Vol. 59, no. 3, pp. 443-449, 1988.
76. E. Reboul, "Absorption of vitamin A and carotenoids by the enterocyte: focus on transport proteins," Nutrients, Vol. 5, no. 9, pp. 3563-3581, 2013.
77. R. Blomhoff and K. Wake, "Perisinusoidal stellate cells of the liver: important roles in retinol metabolism and fibrosis," The FASEB Jour nal, Vol. 5, no. 3, pp. 271-277, 1991.
78. S. Fargion, M. Porzio, and A. L. Fracanzani, "Nonalcoholic fatty liver disease and vascular disease: state-of-the-art," World Journal of Gastroenterology, Vol. 20, pp. 13306-13324, 2014.
79. R. Kleemann, L. Verschuren, M. J. Van Erk et al., "Atherosclerosis and liver inflammation induced by increased dietary cholesterol intake: a combined transcriptomics and metabolomics analysis," Genome Biology, Vol. 8, article R200, 2007.
80. L. Gatica, S. Alvarez, N. Gomez et al., "Vitamin A deficiency induces prooxidant environment and inflammation in rat aorta," Free Radical Research, Vol. 39, no. 6, pp. 621-628, 2005.
81. D. N. D'Ambrosio, R. D. Clugston, and W. S. Blaner, "Vitamin A metabolism: an update," Nutrients, Vol. 3, no. 1, pp. 63-103, 2011.
82. G. P. Lobo, J. Amengual, H. N. Li et al., "β,β-carotene decreases peroxisome proliferator receptor γ activity and reduces lipid storage capacity of adipocytes in a β,β-carotene oxygenase 1-dependent manner," The Journal of Biological Chemistry, Vol. 285, no. 36, pp. 27891-27899, 2010.