Bioactive compounds in food plants and their impact on human health
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1 Bioactive compounds in food plants and their impact on human health Lars Porskjær Christensen Institute for Chemical Engineering, Biotechnology and Environmental Technology, Faculty of Engineering, University of Southern Denmark Spinach Carrots Thyme Elderberries Bioactive natural products in plants Plants produce secondary metabolites mainly for the protection against attack from microorganisms, herbivores etc. > secondary metabolites have so far been isolated from plants. Potential bioactive compounds. Plants can contain > secondary metabolites. Bioactive secondary metabolites from plants: Fatty acid derivatives (e.g., glycolipids such as galactolipids, fatty acids, polyacetylenes). rigin: Acetate pathway. Terpenoids and steroids. rigin: Build up by isoprene units (C 5 ). Polyphenols (e.g., flavonoids, isoflavones, anthocyanins, stilbenes, phenolic acids, lignans). rigin: shikimic acid and/or acetate pathway. Alkaloids. rigin: Derived from amino acids + other pathways Glucosinolates and cyanogenic glycosides. rigin: Derived from amino acids.
2 Characteristics of bioactive natural products Mode of action Bioavailability Absorption from the gastrointestinal tract into plasma. Bioactive compounds has to be relative hydrophobic to be absorbed through the lipophilic cell membrane layers. Binding to specific receptors (i) Size and shape resemblance those of endogen metabolites being able to bind to specific receptors. (ii) Induction/inhibition of specific genes/enzymes/metabolites resulting in a physiological response. Inhibition of ion-channels and disruption of cell membranes Antioxidant activity (i) Direct antioxidant activity. Redox active compounds that inactivate reactive oxygen species (RS). Particular relevant in the prevention of cardiovascular diseases. (ii) Indirect antioxidant activity. Compounds (not necessarily redox active), which induces the production of cytoprotective proteins (phase 2 enzymes). Covalent binding to biomolecules Apoptosis (programme cell death), inhibition of cell proliferation, inhibition of metabolic processes, immune system stimulation. Bioactive compounds in food plants Fatty acid derivatives α-linolenic acid Linoleic acid Bioactivity: Essential fatty acids. Precursor for prostaglandins that are important regulators of metabolic processes. Source: Rapeseed, soya and flaxseed oil and many other plants. CH 2 H CH 2 H C H 2 C Spinach Monogalactosyldiacylglycerol (galactolipid) Bioactivity: Anti-inflammatory and anticancer activity in vitro. In vivo activity unknown (bioavailable?). Source: Mainly green vegetables.
3 Bioactive compounds in food plants Fatty acid derivatives H Carrots Falcarinol (= Panaxynol) Celeriac H Falcarindiol Celery H Panaxydiol Bioactivity: Anti-inflammatory, anticancer, anti-platelet-aggregatory, anti-bacterial, antifungal and more. Mode of action: Covalent-binding to biomolecules (strong alkylating agents). Source: Food plants of the Apiaceae (Umbelliferae) family. Bioactive compounds in food plants Terpenoids Thyme Monoterpenes (C 10 ) Limonene ( )-Menthol Thymol ( )-α-bisabolol H Lactucin Sesquiterpenes (C 15 ) Lettuce H HC H Diterpenes (C 20 ) Carnosoic acid Carnosol C 2 H Steviol Sweet leaf Bioactivity: Anti-inflammatory, anti-bacterial, anti-fungal, and anti-diabetic activity. Mode of action: Disruption of membranes, covalent binding to biomolecules, and binding to specific receptors. Source: Mainly herbs and spices.
4 Bioactive compounds in food plants Triterpenoids Cucurbitacins present in cucumber, melon, and marrow. Bitter tasting, purgative and extremely cytotoxic. Ac H Cucurbitacin E Cucumber Marrow Limonoids present in citrus fruits, seeds, and juice. Bitter tasting and antifeedant activity. Anticancer effect and prevent cardiovascular diseases (reduces LDL cholesterol levels). Ac Limonin Nomilin Bioactive compounds in food plants Tetraterpenes Carotenoids are widespread in plants and have provitamin A activity, antioxidant capacity, and possible anticancer effect (e.g., lycopene) β-carotene (orange) Carrots H Lutein (yellow) Lycopene (red) Tetraterpenes (Carotenoids, C 40 ) Tomatoes
5 Bioactive compounds in food plants Flavonoids H -Glc Rha Glc 4' ' C 6 -C 3 -C 6 flavonoid skeleton Quercetin 3--rutinoside (rutin, flavonol) Luteolin 3--glucoside (flavone) CH 3 Glc H Hesperetin 7--rutinoside (flavanone) (+)-Catechin (flavan-3-ol) Green tea Bioactivity: Antioxidants. Anti-inflammatory, anticancer and immunostimulatory effect and prevention of cardiovascular diseases? Glycosides low bioavailability. Source: Widely distributed in plants. Lemon Bioactive compounds in food plants Isoflavones H H Daidzein Genistein Soybean (Glycine max) Glc Glc Daidzein 7--glucoside Genistein 7--glucoside Phyto-oestrogen Daidzein Bioactivity: Regulates oestrogenic response being able to bind to oestrogen receptors. Prevent the incidence of breast cancer and prostate cancer. Effect against type 2 diabetes? Source: Legumes (in particular soybeans). H H estradiol Steroidal oestrogen
6 Bioactive compounds in food plants Anthocyanins H + H + Glc Glc-Rha Cyanidin 3--glucoside Delphinidin 3--rutinoside Elderberry Blackcurrant Bioactivity: Antioxidants. Anti-inflammatory and anticancer activity and prevention of cardiovascular diseases? Low bioavailability. Source: Widely distributed in plants and present in high concentrations in berries. Bioactive compounds in food plants Stilbenes H trans-resveratrol Red grapes Glc Itadori plant (Japanese knotweed) trans-resveratrol 3--glucoside Bioactivity: Antioxidant, anti-inflammatory and anticancer activity. Prevent the development of cardiovascular diseases (inhibiting LDL-oxidation and platelet aggregation). Source: Grapes, wine, soya and peanut products and in the Itadori plant (roots used to produce tea in Asia). Peanuts
7 Bioactive compounds in food plants Gingerols and Curcuminoids Bioactivity: Anti-inflammatory, antiulcer and anticancer activity. Source: Ginger family (Zingiberaceae) Me H 6-Gingerol Ginger (Zingiber officinale) Curry powder Me Me H Curcumin Turmeric (Curcuma longa) Bioactive compounds in food plants Phenolic acids HC Gallic acid (e.g., red grapes) HC Caffeoylquinic acid (widespread) Red grapes H H C CH 3 CH 3 regano Rosmarinic acid (herbs and spices) 8--4' Diferulic acid (cereals) Bioactivity: Antioxidants. Prevents the development of cardiovascular diseases. Anticancer and immunostimulatory effect? Bioavailable? Cereals
8 Bioactive compounds in food plants Alkaloids N Potato R α-solanine, R = Glucose Rhamnose Galactose Tomato α-chaconine, R = Glucose Rhamnose Galactose Glycoalkaloids (steroidal alkaloids) Bioactivity: Toxic to humans in high concentrations. Potential anticancer effect in low concentrations. Source: Many plants of the genus Solanum (Solanaceae), including potatoes and tomatoes. Bioactive compounds in food plants Glucosinolates N H Glucobrassicin S-Glc N _ S3 K + H N H Indol-3-carbinol (IC3) Anticancer effect Potent inducers of detoxification enzymes resulting in excretion of potential carcinogens prior to harmful effects. Removal of xenobiotics. Antiproliferative effects on cancer cells (apoptosis). Phyto-oestrogenic effect. Prevention of breast/prostate cancer (IC3). CH 2 CH 2 R S-Glucose Myrosinase S C N R CH N 2 S- 3 K + Glucose Sulphate Isothiocyanates Glucosinolates Anticancer effect S
9 State of the art within the field of bioactive compounds in food plants Direct antioxidants (especially glycosides) are not major contributors to the health effects of plant-based foods due to: (i) low bioavailability, (ii) metabolization and absorption in vivo unclear, (iii) general low bioactivity compared to other bioactive compounds etc. Health effects of plant-based foods are most likely due to the presence of bioactive compounds with bioactivity unrelated to antioxidant activity. Hypotheses Bioactive secondary metabolites with different bioactivities and mode of actions are major contributors to the health promoting effects of plant-based foods. Future work (i) Focus on identification of highly bioactive compounds with effects towards specific diseases and their possible mode of action. (ii) Bioavailability and metabolization of bioactive compounds. Bioactive compounds in plants: Anticancer effect and other health promoting effects of carrots Carrots are used for foods all over the world and have been used in centuries in traditional medicine in the West. Carrot is closely related with food plants and medicinal plants of the Apiaceae and Araliaceae plant families that are known to possess important pharmacological effects such as: Anti-inflammatory effect Carrots Anticancer effect Anti-platelet-aggregatory effects Anti-diabetic effects... and many other pharmacological effects
10 Anticancer effect of carrots Epidemiological studies have shown that the intake of vegetables rich in α- and β-carotene, and/or a high level of β-carotene in blood samples, is correlated with a reduced risk of cancer. Intake of α- and β-carotene is closely correlated with a high intake of carrots. Human intervention studies: supplements of β-carotene increased the incidence of cancer! β -Carotene paradox Do carrots contain other potential substances with the ability to prevent cancer? Potential bioactive compounds of carrots Monoterpenes p-cymene Terpinolene Limonene γ-terpinene H H Sesquiterpenes β-caryophyllene (E)-γ-bisabolene Tetraterpenes β-carotene
11 Potential bioactive compounds of carrots Anti-fungal Cytotoxic H 3 C H 3 C Anti-inflammatory 2-Epilaserine H 6-Methoxymellein Anti-inflammatory? Antioxidant? + H 3 C CH CH 3 Gazarin CH 3 + other cyanidin derivatives Glc Cyanidin 3--glucoside Potential bioactive compounds of carrots H Falcarinol (= Panaxynol) H Falcarindiol H 3 CC Falcarindiol 3-acetate H Panaxydiol
12 Bioassay-guided fractionation for identification of potential anticancer principles of carrots Processing/extraction Methanol extract Testing for effects in relevant in vitro bioassays: (i) Anticancer (ii) Anti-inflammatory (iii) Antibiotic (iv) Anti-diabetic Etc. H Fractionation and testing Falcarinol (= Panaxynol) H Falcarindiol Potential anticancer and antiinflammatory principles in carrots + Effect of falcarinol and falcarindiol on the proliferation of human colon cancer cells (Caco-2) Fluorescense (viability) 350 x x x Falcarindiol Falcarinol x K 0,625% FCS 0 ppb 1 ppb 10 ppb 100 ppb 1 ppm 2,5 ppm 5 ppm 10 ppm 20 ppm Concentration (μg/ml) Larsen, Purup & Christensen (2009). J. Agric. Food Chem. 57,
13 Effect of falcarinol and falcarindiol on the proliferation of normal small intestinal cells 800 x Falcarindiol Fluorescense (viability) x x x Falcarinol K 0,625% FCS 0 ppb 1 ppb 10 ppb 100 ppb 1 ppm 2,5 ppm 5 ppm 10 ppm 20 ppm Concentration (μg/ml) Larsen, Purup & Christensen (2009). J. Agric. Food Chem. 57, Effects of falcarinol on cell proliferation of normal cells and Caco-2 cells Stimulating effect 1,5 1.5 Effect on cell proliferation of primary Effect mammary on cell proliferation epithelial cells ,5 Inhibiting effect ** *** No effect P < 0.09 ** P < 0.01 *** P < Falcarinol (μg/ml) Hansen et al. (2003). J. Sci. Food Agric. 83, ; Young et al. (2007). J. Agric. Food Chem. 55,
14 Effects of β-carotene on cell proliferation of normal and Caco-2 cells Effect on cell proliferation of primary Effect mammary on cell epithelial proliferation cells No effect β-carotene (ng/ml) Hansen et al. (2003). J. Sci. Food Agric. 83, Bioavailability of polyacetylenes determined by multiple reaction monotioring (MRM) LC-MS/MS Plasma samples plasma+0 fc Sm (Mn, 2x3) 100 Mass transition m/z 227 [M + H H 2 ] + m/z 91 Falcarinol standard (3.3 ng/ml) Standard: 3.3 ng/ml Falcarinol MRM of 2 Channels ES > e3 % fc Sm (Mn, 2x3) 100 Plasma + falcarinol Plasma added 3.3 ng/ml 7.20 MRM of 2 Channels ES+ 227 > e3 Proteins removed by precipitation with acetonitrile % fc Sm (Mn, 2x3) 100 Plasma blank Plasma blank MRM of 2 Channels ES+ 227 > e3 % Time Christensen & Brandt (2006). J. Pharm. Biomed. Anal. 41,
15 Bioavailability studies of falcarinol in humans Concentration of falcarinol in plasma as function of time after ingestion of a breakfast meal consisting of carrot juice (13 mg/l). n = Falcarinol (ng/ml) ml juice 600 ml juice 300 ml juice Time (hours) Brandt et al. (2004). Trends Food Sci. Technol. 15, Potential anticancer effect of carrots and polyacetylenes demonstrated in rats induced with colon cancer Male BDIX (rat model) ACF (»Aberrant Crypt Foci«) = biomarkers for advanced steps on the progression towards cancer ACF = 5 Tumours in rat colon
16 Effect of treatments with carrot or falcarinol in physiological relevant concentrations of four types of (pre)cancerous lesions in rat colons Standard rat feed + 10% freeze-dried carrots Normalised effect of treatments Carrot Falcarinol % of mean number in control treatment Linear (carrot) ---- Linear (falcarinol) 0 Small ACF (1 3) Medium ACF (4 6) Large ACF (> 7) Tumours ( 1 mm) Type and size of lesion Standard rat feed + 10% maize starch (control) Increasing steps on the progression towards cancer. The trend for reducing the size of lesion was significant (P = 0.028) Kobæk-Larsen et al. (2005). J. Agric. Food Chem. 53, Falcarinol-type polyacetylenes strong alkylating agents H H + + H 2 Falcarinol H 2 R HS+ RSH + H + Resonance stabilised carbocation R S Falcarinol coupled to biomolecules (e.g., a protein)
17 Effect of falcarinol and falcarinon on the proliferation of human colon cancer cells (Caco-2) 120 V ia bility (re la tiv e ) H Falcarinon Falcarinol Concentration (μg/ml) Larsen, Purup & Christensen (2009). J. Agric. Food Chem. 57, Health promoting effects of falcarinol-type polyacetylenes probably related to their lipophilic and alkylating properties Immunomodulatory effect: Enhanced production of T-lymphocytes and macrophages through interaction with proteins, e.g., formation of haptenprotein complexes (antigens). Inactivation of proteins/enzymes: (i) Inhibition of enzymes responsible for the proliferation of cancer cells such as CX-2 and nuclear factor κb. Anti-inflammatory activity! (ii) Inhibition of CX-1 and CX-2 related to the anti-inflammatory effect of falcarinol-type polyacetylenes, and hence also their possible anti-platelet aggregatory effects. Regulation of prostaglandin production. Apoptosis (programme cell death). (i) DNA damage. (ii) Induction of cell cycle arrest. (iii) Cell damage caused by increased production of macrophages.... and many other possible explanations.
18 Thank you for your attention!
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