Differential bioavailability, clearance, and tissue distribution of the acyclic tomato carotenoids lycopene and phytoene in mongolian gerbils.

Lycopene (LYC) is the major tomato carotenoid and is the focus of substantial research. Phytoene (PE), a minor tomato carotenoid, is found in human blood and tissues in similar concentrations to LYC. To determine which metabolic differences underlie this phenomenon, Mongolian gerbils (Meriones unguiculatus, n = 56) were fed control or tomato powder (TP)-containing diets (to establish steady-state serum and tissue carotenoid concentrations similar to tomato-fed humans) for 26 d. The TP-fed gerbils were then provided either a single, oral, cottonseed oil (CO) vehicle dose and tissues were collected at 6 h or they were provided unlabeled PE or LYC in CO and tissues were evaluated at 6, 12, or 24 h. In vehicle-dosed, TP-fed gerbils, LYC was the major carotenoid (≥ 55% carotenoids) in liver, spleen, testes, and the prostate-seminal vesicle complex, whereas PE was the major serum and adipose carotenoid (≥ 37% total carotenoid) and phytofluene was the major carotenoid (≥ 38%) in adrenals and lungs. PE dosing increased hepatic, splenic, and serum PE concentrations compared with vehicle dosing (P < 0.05) from 6 to 24 h, whereas LYC dosing increased only serum LYC at 6 and 12 h (P < 0.05) compared with vehicle dosing. This suggested PE was more bioavailable and cleared more slowly than LYC. To precisely track absorptive and distributive differences, (14)C-PE or (14)C-LYC (n = 2/group) was provided to TP-fed gerbils. Bioavailability assessed by carcass (14)C-content was 23% for PE and 8% for LYC. Nearly every extra-hepatic tissue accumulated greater dose radioactivity after (14)C-PE than (14)C-LYC dosing. Thus, LYC and PE, which structurally differ only by saturation, pharmacokinetically differ in bioavailability, tissue deposition, and clearance.

[1]  J. Erdman,et al.  Complex interactions between dietary and genetic factors impact lycopene metabolism and distribution. , 2013, Archives of biochemistry and biophysics.

[2]  M. Lila,et al.  Biosynthesis of highly enriched 13C-lycopene for human metabolic studies using repeated batch tomato cell culturing with 13C-glucose. , 2013, Food chemistry.

[3]  B. Clevidence,et al.  Strong and weak plasma response to dietary carotenoids identified by cluster analysis and linked to beta-carotene 15,15'-monooxygenase 1 single nucleotide polymorphisms. , 2013, The Journal of nutritional biochemistry.

[4]  R. Vasan,et al.  Relationship of lycopene intake and consumption of tomato products to incident CVD , 2013, British Journal of Nutrition.

[5]  T. Mäkikallio,et al.  Low serum lycopene and β-carotene increase risk of acute myocardial infarction in men. , 2012, European journal of public health.

[6]  K. Ronkainen,et al.  Serum lycopene decreases the risk of stroke in men , 2012, Neurology.

[7]  O. Dangles,et al.  Effects of physicochemical properties of carotenoids on their bioaccessibility, intestinal cell uptake, and blood and tissue concentrations. , 2012, Molecular nutrition & food research.

[8]  J. Erdman,et al.  Coconut oil enhances tomato carotenoid tissue accumulation compared to safflower oil in the Mongolian gerbil ( Meriones unguiculatus ). , 2012, Journal of agricultural and food chemistry.

[9]  Edward L. Giovannucci,et al.  Lycopene, Tomato Products, and Prostate Cancer Incidence: A Review and Reassessment in the PSA Screening Era , 2012, Journal of oncology.

[10]  Yong‐Su Jin,et al.  Laboratory-scale production of 13C-labeled lycopene and phytoene by bioengineered Escherichia coli. , 2011, Journal of agricultural and food chemistry.

[11]  H. Synal,et al.  Lycopene bioavailability and metabolism in humans: an accelerator mass spectrometry study. , 2011, The American journal of clinical nutrition.

[12]  J. Erdman,et al.  Nutritional aspects of phytoene and phytofluene, carotenoid precursors to lycopene. , 2011, Advances in nutrition.

[13]  J. von Lintig,et al.  Loss of carotene-9',10'-monooxygenase expression increases serum and tissue lycopene concentrations in lycopene-fed mice. , 2010, The Journal of nutrition.

[14]  M. Lila,et al.  Screening and selection of high carotenoid producing in vitro tomato cell culture lines for [13C]-carotenoid production. , 2010, Journal of agricultural and food chemistry.

[15]  E. Harrison,et al.  Identification and quantification of apo-lycopenals in fruits, vegetables, and human plasma. , 2010, Journal of agricultural and food chemistry.

[16]  M. Lila,et al.  Herbicide treatments alter carotenoid profiles for 14C tracer production from tomato ( Solanum lycopersicum cv. VFNT cherry) cell cultures. , 2009, Journal of agricultural and food chemistry.

[17]  J. Erdman,et al.  Absorption, transport, distribution in tissues and bioavailability. , 2009 .

[18]  K. Jamil,et al.  Sweet potato beta-carotene bioefficacy is enhanced by dietary fat and not reduced by soluble fiber intake in Mongolian gerbils. , 2009, The Journal of nutrition.

[19]  M. Lila,et al.  Optimization of lycopene extraction from tomato cell suspension culture by response surface methodology. , 2008, Journal of agricultural and food chemistry.

[20]  E. Reboul,et al.  Lycopene absorption in human intestinal cells and in mice involves scavenger receptor class B type I but not Niemann-Pick C1-like 1. , 2008, The Journal of nutrition.

[21]  M. Lila,et al.  Phytoene, Phytofluene, and Lycopene from Tomato Powder Differentially Accumulate in Tissues of Male Fisher 344 Rats. , 2007, Nutrition research.

[22]  V. Böhm,et al.  Isolation and structural elucidation of different geometrical isomers of lycopene. , 2007, International journal for vitamin and nutrition research. Internationale Zeitschrift fur Vitamin- und Ernahrungsforschung. Journal international de vitaminologie et de nutrition.

[23]  P. Simon,et al.  Beta-carotene from red carrot maintains vitamin A status, but lycopene bioavailability is lower relative to tomato paste in Mongolian gerbils. , 2007, The Journal of nutrition.

[24]  S. Clinton,et al.  Carotenoid absorption in humans consuming tomato sauces obtained from tangerine or high-beta-carotene varieties of tomatoes. , 2007, Journal of agricultural and food chemistry.

[25]  Brian L. Lindshield,et al.  Combinations of tomato and broccoli enhance antitumor activity in dunning r3327-h prostate adenocarcinomas. , 2007, Cancer research.

[26]  C. Chuang,et al.  Effects of lycopene supplementation on plasma and tissue lycopene levels in various rodent strains. , 2006, International journal for vitamin and nutrition research. Internationale Zeitschrift fur Vitamin- und Ernahrungsforschung. Journal international de vitaminologie et de nutrition.

[27]  W. Koff,et al.  Effect of the consumption of tomato paste on plasma prostate-specific antigen levels in patients with benign prostate hyperplasia. , 2006, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[28]  J. Erdman,et al.  Apo-8'-lycopenal and apo-12'-lycopenal are metabolic products of lycopene in rat liver. , 2006, The Journal of nutrition.

[29]  M. Lila,et al.  Biosynthesis of 14C-phytoene from tomato cell suspension cultures (Lycopersicon esculentum) for utilization in prostate cancer cell culture studies. , 2006, Journal of agricultural and food chemistry.

[30]  E. Harrison,et al.  Carotenoid transport is decreased and expression of the lipid transporters SR-BI, NPC1L1, and ABCA1 is downregulated in Caco-2 cells treated with ezetimibe. , 2005, The Journal of nutrition.

[31]  J. Erdman,et al.  The biodistribution of a single oral dose of [14C]-lycopene in rats prefed either a control or lycopene-enriched diet. , 2005, The Journal of nutrition.

[32]  John W Erdman,et al.  The tomato as a functional food. , 2005, The Journal of nutrition.

[33]  G. Sandmann,et al.  ζ-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene , 2005, Planta.

[34]  Brian L. Lindshield,et al.  Tomato phytochemicals and prostate cancer risk. , 2004, The Journal of nutrition.

[35]  M. Etminan,et al.  The role of tomato products and lycopene in the prevention of prostate cancer: a meta-analysis of observational studies. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[36]  S. Lemeshow,et al.  Prostate carcinogenesis in N-methyl-N-nitrosourea (NMU)-testosterone-treated rats fed tomato powder, lycopene, or energy-restricted diets. , 2004, Journal of the National Cancer Institute.

[37]  M. Lila,et al.  [14C]-lycopene and [14C]-labeled polar products are differentially distributed in tissues of F344 rats prefed lycopene. , 2003, The Journal of nutrition.

[38]  Da-You Zhao,et al.  Chemistry, Distribution, and Metabolism of Tomato Carotenoids and Their Impact on Human Health , 2002, Experimental biology and medicine.

[39]  S. Hessel,et al.  Identification and Characterization of a Mammalian Enzyme Catalyzing the Asymmetric Oxidative Cleavage of Provitamin A* , 2001, The Journal of Biological Chemistry.

[40]  C. Fjeld,et al.  Food, phytonutrients, and health: rationale for the conference and workshops. , 2009, Nutrition reviews.

[41]  B. Clevidence,et al.  Carotenoids in human buccal mucosa cells after 4 wk of supplementation with tomato juice or lycopene supplements. , 1999, The American journal of clinical nutrition.

[42]  H. van den Berg Carotenoid interactions. , 1999, Nutrition reviews.

[43]  D. Rodriguez-Amaya A Guide to Carotenoid Analysis in Foods , 1999 .

[44]  F. Khachik,et al.  Chronic ingestion of lycopene-rich tomato juice or lycopene supplements significantly increases plasma concentrations of lycopene and related tomato carotenoids in humans. , 1998, The American journal of clinical nutrition.

[45]  P. Fraser,et al.  Expression of an active phytoene synthase from Erwinia uredovora and biochemical properties of the enzyme. , 1998, Biochimica et biophysica acta.

[46]  D. Bostwick,et al.  cis-trans lycopene isomers, carotenoids, and retinol in the human prostate. , 1996, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[47]  G. Britton,et al.  Isolation and analysis , 1995 .

[48]  J. Graham,et al.  Isolation and analysis , 1993 .

[49]  W. Stahl,et al.  cis-trans isomers of lycopene and β-carotene in human serum and tissues , 1992 .

[50]  W. Stahl,et al.  cis-trans isomers of lycopene and beta-carotene in human serum and tissues. , 1992, Archives of biochemistry and biophysics.

[51]  J. Erdman,et al.  Concentrations of selected carotenoids and vitamin A in human liver, kidney and lung tissue. , 1991, The Journal of nutrition.

[52]  L. Kaplan,et al.  Carotenoid composition, concentrations, and relationships in various human organs. , 1990, Clinical physiology and biochemistry.

[53]  R. Nicolosi,et al.  Effect of dietary fat on hepatic metabolism of 14C-oleic acid and very low density lipoprotein triglyceride in the gerbil. , 1976, The Journal of nutrition.