Genetic ablation of carotene oxygenases and consumption of lycopene or tomato powder diets modulate carotenoid and lipid metabolism in mice

Nutrition Research

Volumn 33, Issue 9, 2013, Pages 733-742

  Ford, Nikki A ^a   Elsen, Amy C ^b   Erdman, John W ^b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cholesterol; CMO I; CMO II; Lipids; Lycopene; Mice; Phytoene; Tomato

Indexed keywords

CAROTENE 15,15' MONOOXYGENASE; CAROTENE 9',10' MONOOXYGENASE; CAROTENOID; CHOLESTEROL; GLUCOSE; INSULIN; LEPTIN; LIPID; LYCOPENE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; SOMATOMEDIN C; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEEDING; FEMALE; FOOD INTAKE; GENETIC ABLATION; GENETIC PROCEDURES; GENOTYPE; LIPID METABOLISM; LIPIDOSIS; LIVER; MOUSE; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TOMATO; VITAMIN METABOLISM; WILD TYPE;

LYCOPERSICON ESCULENTUM; MAMMALIA; MUS;

CAROTENE-15,15′-MONOOXYGENASE; CAROTENE-9′,10′-MONOOXYGENASE; CHOLESTEROL; CMO-I; CMO-II; IGF-1; INSULIN-LIKE GROWTH FACTOR 1; LIPIDS; LYCOPENE; MESSENGER RNA; MICE; MRNA; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PHYTOENE; PPAR; RETINOID X RECEPTOR; RXR; SINGLE NUCLEOTIDE POLYMORPHISM; SNP; TOMATO; WILD-TYPE; WT;

ADIPOSE TISSUE; ANIMALS; BETA CAROTENE; BETA-CAROTENE 15,15'-MONOOXYGENASE; CAROTENOIDS; CHOLESTEROL; DIET; FATTY ACID DESATURASES; FEMALE; GENOTYPE; HORMONES; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR I; LIPID METABOLISM; LIVER; LYCOPERSICON ESCULENTUM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SIZE; PHENOTYPE; POWDERS; RNA, MESSENGER;

EID: 84883805355     PISSN: 02715317     EISSN: 18790739     Source Type: Journal    
DOI: 10.1016/j.nutres.2013.07.007     Document Type: Article

References (49)

1. Monsen E.R. Dietary reference intakes for the antioxidant nutrients: vitamin C, vitamin E, selenium, and carotenoids. J Am Diet Assoc 2000, 100:637-640.
2. Britton G., Liaaen-Jensen S., Pfander H. Carotenoids 1995, 1A:328.
3. Goodman D.S., Huang H.S., Shiratori T. Mechanism of the biosynthesis of vitamin A from beta-carotene. J Biol Chem 1966, 241:1929-1932.
4. Britton G., Liaaen-Jensen S., Pfander H. Carotenoids 2009, 5:328.
5. Lindqvist A., Andersson S. Biochemical properties of purified recombinant human beta-carotene 15,15'-monooxygenase. J Biol Chem 2002, 277:23942-23948.
6. Hu K., Liu C., Ernst H., Krinsky N., Russell R., Wang X. The biochemical characterization of ferret carotene-9',10'-monooxygenase catalyzing cleavage of carotenoids in vitro and in vivo. J Biol Chem 2006, 281:19327-19338.
7. Kiefer C., Hessel S., Lampert J.M., Vogt K., Lederer M.O., Breithaupt D.E., et al. Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J Biol Chem 2001, 276:14110-14116.
8. Amengual J., Lobo G., Golczak M., Li H.N.M., Klimova T., Hoppel C., et al. A mitochondrial enzyme degrades carotenoids and protects against oxidative stress. FASEB J 2011, 25:948-959.
9. Wang X.D. Lycopene metabolism and its biological significance. Am J Clin Nutr 2012, 96:1214S-1222S.
10. Lietz G., Oxley A., Boesch Saadatmandi C., Kobayashi D. Importance of β, β-carotene 15,15'-monooxygenase 1 (BCMO1) and β, β-carotene 9',10'-dioxygenase 2 (BCDO2) in nutrition and health. Mol Nutr Food Res 2012, 56:241-250.
11. Sharoni Y., Linnewiel-Hermoni K., Khanin M., Salman H., Veprik A., Danilenko M., et al. Carotenoids and apocarotenoids in cellular signaling related to cancer: a review. Mol Nutr Food Res 2012, 56:259-260.
12. Erdman J.W., Ford N.A., Lindshield B.L. Are the health attributes of lycopene related to its antioxidant function?. Arch Biochem Biophys 2009, 483:229-235.
13. Hessel S., Eichinger A., Isken A., Amengual J., Hunzelmann S., Hoeller U., et al. CMO1 deficiency abolishes vitamin A production from beta-carotene and alters lipid metabolism in mice. J Biol Chem 2007, 282:33553-33561.
14. Poulsen L.L.C., Siersbk M., Mandrup S. PPARs: fatty acid sensors controlling metabolism. Sem in Cell Dev Bio 2012, 23:631-639.
15. Huang J., Jia Y., Fu T., Viswakarma N., Bai L., Rao M.S., et al. Sustained activation of PPARalpha by endogenous ligands increases hepatic fatty acid oxidation and prevents obesity in ob/ob mice. FASEB J 2012, 26:628-630.
16. Boulanger A., McLemore P., Copeland N., Gilbert D., Jenkins N., Yu S., et al. Identification of beta-carotene 15, 15'-monooxygenase as a peroxisome proliferator-activated receptor target gene. FASEB 2003, 17:1304-1306.
17. Zaripheh S., Nara T., Nakamura M., Erdman J.W. Dietary lycopene downregulates carotenoid 15,15'-monooxygenase and PPAR-gamma in selected rat tissues. J Nutr 2006, 136:932-938.
18. Tontonoz P., Hu E., Graves R.A., Budavari A.I., Spiegelman B.M. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Devel 1994, 8:1224-1230.
19. Lobo G.P., Hessel S., Eichinger A., Noy N., Moise A.R., Wyss A., et al. ISX is a retinoic acid-sensitive gatekeeper that controls intestinal beta, beta-carotene absorption and vitamin A production. FASEB J 2010, 24:1656-1660.
20. Eroglu A., Hruszkewycz D.P., dela Sena C., Narayanasamy S., Riedl K.M., Kopec R.E., et al. Naturally occurring eccentric cleavage products of provitamin A beta-carotene function as antagonists of retinoic acid receptors. J Biol Chem 2012, 287:15886-15895.
21. Eroglu A., Hruszkewycz D.P., Curley R.W., Harrison E.H. The eccentric cleavage product of beta-carotene, beta-apo-13-carotenone, functions as an antagonist of RXRalpha. Arch Biochem Biophys 2010, 504:11-16.
22. Takitani K., Miyazaki H., Takaya R., Tamai H. Expression of beta-carotene 15,15'-monooxygenase gene and retinol status in type 2 diabetic Goto-Kakizaki rats. Biofactors 2008, 33:77-83.
23. Coyne T., Ibiebele T.I., Baade P.D., McClintock C.S., Shaw J.E. Metabolic syndrome and serum carotenoids: findings of a cross-sectional study in Queensland, Australia. Br J Nutr 2009, 102:1668-1677.
24. Ford N., Clinton S., von Lintig J., Wyss A., Erdman J.W. Loss of carotene-9',10'-monooxygenase expression increases serum and tissue lycopene concentrations in lycopene-fed mice. J Nutr 2010, 140:2134-2138.
25. Boileau T.W., Clinton S.K., Zaripheh S., Monaco M.H., Donovan S.M., Erdman J.W. Testosterone and food restriction modulate hepatic lycopene isomer concentrations in male F344 rats. J Nutr 2001, 131:1746-1752.
26. Campbell J., Engelmann N., Lila M., Erdman J.W. Phytoene, phytofluene, and lycopene from tomato powder differentially accumulate in tissues of male fisher 344 rats. Nutr Res 2007, 27:794-801.
27. Yeum K.J., Booth S.L., Sadowski J.A., Liu C., Tang G., Krinsky N.I., et al. Human plasma carotenoid response to the ingestion of controlled diets high in fruits and vegetables. Am J Clin Nutr 1996, 64:594-602.
28. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226:497-509.
29. Lindshield B., King J., Wyss A., Goralczyk R., Lu C., Ford N., et al. Lycopene biodistribution is altered in 15,15'-carotenoid monooxygenase knockout mice. J Nutr 2008, 138:2367-2371.
30. Harrison E.H., dela Sena C., Eroglu A., Fleshman M.K. The formation, occurrence, and function of beta-apocarotenoids: beta-carotene metabolites that may modulate nuclear receptor signaling. Am J Clin Nutr 2012, 96:1189S-1192S.
31. Andreassen M., Raymond I., Kistorp C., Hildebrandt P., Faber J., Kristensen L.Ø. IGF1 as predictor of all-cause mortality and cardiovascular disease in an elderly population. Euro J Endo 2009, 160:25-31.
32. Ernest A., Adem A., Hasan M.Y., Tekes K., Kalasz H. Medicinal chemistry and actions of dual and pan PPAR modulators. Open Med Chem J 2011, 5:93-98.
33. Hursting S.D., Hursting M.J. Growth signals, inflammation, and vascular perturbations: mechanistic links between obesity, metabolic syndrome, and cancer. Arterioscler Thromb Vasc Biol 2012, 32:1766-1770.
34. Ferrucci L., Perry J.R., Matteini A., Perola M., Tanaka T., Silander K., et al. Common variation in the beta-carotene 15,15'-monooxygenase 1 gene affects circulating levels of carotenoids: a genome-wide association study. Am J Hum Genet 2009, 84:123-130.
35. Lindqvist A., Sharvill J., Sharvill D., Andersson S. Loss-of-function mutation in carotenoid 15,15'-monooxygenase identified in a patient with hypercarotenemia and hypovitaminosis A. J Nutr 2007, 137:2346-2350.
36. Leung W.C., Hessel S., Mplan C., Flint J., Oberhauser V., Tourniaire F., et al. Two common single nucleotide polymorphisms in the gene encoding beta-carotene 15,15'-monoxygenase alter beta-carotene metabolism in female volunteers. FASEB J 2009, 23:1041-1053.
37. Lietz G., Oxley A., Leung W., Hesketh J. Single nucleotide polymorphisms upstream from the beta-carotene 15,15'-monoxygenase gene influence provitamin A conversion efficiency in female volunteers. J Nutr 2012, 142:161S-165S.
38. Tourniaire F., Gouranton E., von Lintig J., Keijer J., Bonet M.L., Amengual J., et al. beta-Carotene conversion products and their effects on adipose tissue. Genes Nutr 2009, 4:179-187.
39. Tourniaire F., Minihane A.M., Hesketh J., Lietz G. Do single nucleotide polymorphisms in β-carotene dioxygenase-2 (BCDO2) gene affect the postprandial response?. Proc Nutr Soc 2008, 67.
40. Eriksson J., Larson G., Gunnarsson U., Bed'hom B., Tixier-Boichard M., Stromstedt L., et al. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet 2008, 4:e1000010.
41. Vage D.I., Boman I.A. A nonsense mutation in the beta-carotene oxygenase 2 (BCO2) gene is tightly associated with accumulation of carotenoids in adipose tissue in sheep (Ovis aries). BMC Genet 2010, 11. 10.1186/1471-2156-11-10.
42. Berry S.D., Davis S.R., Beattie E.M., Thomas N.L., Burrett A.K., Ward H.E., et al. Mutation in bovine beta-carotene oxygenase 2 affects milk color. Genetics 2009, 182:923-926.
43. He M., Cornelis M.C., Kraft P., van Dam R.M., Sun Q., Laurie C.C., et al. Genome-wide association study identifies variants at the IL18-BCO2 locus associated with interleukin-18 levels. Arterioscler Thromb Vasc Biol 2010, 30:885-890.
44. Amengual J., Gouranton E., van Helden Y.G.J., Hessel S., Ribot J., Kramer E., et al. Beta-carotene reduces body adiposity of mice via BCMO1. PLoS One 2011, 6:e20644.
45. Villaa-Chaves G., Pereira S., Saboya C., Ramalho A. Non-alcoholic fatty liver disease and its relationship with the nutritional status of vitamin A in individuals with class III obesity. Obesity Surg 2008, 18:378-385.
46. Fuhrman B., Elis A., Aviram M. Hypocholesterolemic effect of lycopene and beta-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages. Biochem Biophys Res Commun 1997, 233:658-662.
47. Sluijs I., Beulens J.W.J., Grobbee D., van der Schouw Y.T. Dietary carotenoid intake is associated with lower prevalence of metabolic syndrome in middle-aged and elderly men. J Nutr 2009, 139:987-992.
48. Lobo G.P., Amengual J., Li H.N., Golczak M., Bonet M.L., Palczewski K., et al. Beta, beta-carotene decreases peroxisome proliferator receptor gamma activity and reduces lipid storage capacity of adipocytes in a beta, beta-carotene oxygenase 1-dependent manner. J Biol Chem 2010, 285:27891-27899.
49. van Helden Y.G., Godschalk R.W., Swarts H.J., Hollman P.C., van Schooten F.J., Keijer J. Beta-carotene affects gene expression in lungs of male and female Bcmo1 (-/-) mice in opposite directions. Cell Mol Life Sci 2011, 68:489-504.