Food Chemistry 161 (2014) 27–39

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Review

Health effects and occurrence of dietary polyamines: A review for the period 2005–mid 2013 Pavel Kalacˇ ⇑ Department of Applied Chemistry, Faculty of Agriculture, University of South Bohemia, 37005 Cˇeské Budeˇjovice, Czech Republic

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Article history: Received 26 November 2013 Received in revised form 31 January 2014 Accepted 20 March 2014 Available online 28 March 2014 Keywords: Food Health effects Polyamines Biogenic amines Spermidine Spermine

a b s t r a c t This review continues a previous one (Kalacˇ & Krausová, 2005). Dietary polyamines spermidine and spermine participate in an array of physiological roles with both favourable and injurious effects on human health. Dieticians thus need plausible information on their content in various foods. The data on the polyamine contents in raw food materials increased considerably during the reviewed period, while information on their changes during processing and storage have yet been fragmentary and inconsistent. Spermidine and spermine originate mainly from raw materials. Their high contents are typical particularly for inner organs and meat of warm-blooded animals, soybean and fermented soybean products and some mushroom species. Generally, polyamine contents range widely within the individual food items. Ó 2014 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3.

4.

5. 6.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamines synthesis, homeostasis and catabolism. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biological roles in man. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Participation in tumour growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Effects on intestinal tract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Antioxidant activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Further effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Toxicity and health risks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Levels in human blood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polyamines in food. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Recent original papers with overall data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Polyamines in foods of plant and mushroom origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.1. Polyamines in cereals, legumes, tubers, vegetables and mushrooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2. Polyamines in fruits and beverages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Polyamines in foods of animal origin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.1. Polyamines in meat, inner organs and meat products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.2. Polyamines in fish, shellfish and seafoods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.3. Polyamines in milk, milk products and eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Intake of dietary polyamines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nutritional evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

⇑ Tel.: +420 387 772 657; fax: +420 385 310 405. E-mail address: [email protected] http://dx.doi.org/10.1016/j.foodchem.2014.03.102 0308-8146/Ó 2014 Elsevier Ltd. All rights reserved.

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P. Kalacˇ / Food Chemistry 161 (2014) 27–39

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1. Introduction The category of biologically active, or physiological, polyamines (PAs) consists of putrescine (PUT; 1,4-diaminobutane), spermidine (SPD; N-(3-aminopropyl)-1,4-diaminobutane) and spermine (SPM; N,N0 -bis-(3-aminopropyl)-1,4-diaminobutane) (Fig. 1). The polyamines were traditionally classified within the group of biogenic amines, however, they have been set apart as a peculiar group since the 1990s, particularly due to their different formation and specific roles in eukaryotic cells. Putrescine, being structurally a diamine, is classified in both groups. It is widely formed as a ‘‘true’’ biogenic amine by the decarboxylation of amino acid ornithine, but it is also an intermediate in SPD and SPM biosynthesis. Nevertheless, biogenic diamine cadaverine produced by enzymatic decarboxylation of lysine does not rank among physiological PAs, similar to agmatine, formed by enzymatic decarboxylation of arginine. The polyamines are ubiquitous, widespread from bacteria to mammals. Their participation in cell growth and proliferation has been of primary interest. The knowledge of the main roles of PAs in health, disease and ageing was reviewed (Larqué, SabaterMolina, & Zamora, 2007; Wallace, 2009), and various aspects of polyamine physiological effects in man were covered in a book by Dandrifosse (2009a). Body pool of the PAs is maintained by three sources: (i) endogenous (de novo) biosynthesis, (ii) production by intestinal bacteria or from constituents of epithelial cells shed into the gut lumen, and (iii) dietary intake. Diet provides a larger daily quantity of PAs than does endogenous biosynthesis. Dietary PAs are completely absorbed, so diet may be a useful source of these substances (Bardócz, 1995). Despite both polyamine daily cellular requirement and optimum levels of dietary intake being until now undetermined, plausible data on PAs content in foods and beverages are necessary for the estimation of their intake. The aim of the review is to collect and evaluate data on dietary PAs published since 2005. The review follows a previous one (Kalacˇ & Krausová, 2005). 2. Polyamines synthesis, homeostasis and catabolism This chapter gives an overall characterisation, as it deals with biochemical and medical topics. Partial reviews will therefore be preferentially cited and the reader is directed to them and the references therein. Polyamine homeostasis in mammalian cells is achieved by a complex network of regulatory mechanisms affecting both synthesis and degradation, as well as membrane transport of PAs. Depletion of cellular PAs rapidly induces an increased uptake of exogenous PAs, whereas an excess of PAs down-regulates the polyamine transporter(s). Polyamine biosynthesis is an ancient metabolic pathway present in all living organisms. Their homeostasis is necessary for cell

Fig. 2. A simplified scheme of polyamine biosynthesis pathways (Kalacˇ, 2010). The pathway via agmatin, known in bacteria and plants, was proposed also for mammals. Methionine is a donor of aminopropyl unit for spermidine and spermine formation. Putrescine is an intermediate of spermidine and spermine biosynthesis. Participating enzymes: (1) arginase (EC 3.5.3.1); (2) ornithine decarboxylase (EC 4.1.1.17); (3) arginine decarboxylase (EC 4.1.1.19); (4) agmatinase (EC 3.5.3.11); (5) spermidine synthase (EC 2.5.1.16); (6) spermine synthase (EC 2.5.1.22); (7) adenosyltransferase (EC 2.5.1.6); (8) S-adenosyl-L-methionine decarboxylase (EC 4.1.1.50).

survival. Its deregulation is involved in illnesses, such as cancer or neurodegenerative disorders. In healthy cells, PAs level are intricately controlled by biosynthesis and catabolic enzymes (Pegg, 2009). The biosynthesis uses the amino acids arginine, ornithine and methionine. A simplified scheme is given in Fig. 2. The pathway starts with the production of ornithine from arginine by the mitochondrial enzyme arginase. Ornithine is then decarboxylated by one of the key enzymes, ornithine decarboxylase, to produce PUT. In parallel to PUT formation, L-methionine is converted into S-adenosyl-L-methionine (AdoMet). It is then decarboxylated by another key enzyme, S-adenosyl-L-methionine decarboxylase, to produce decarboxylated AdoMet. This compound is then used as a donor of aminopropyl group to either PUT (by spermidine synthase) to produce SPD, or to SPD to produce SPM (by spermine synthase). SPD and SPM can be converted back to PUT. The rate-limiting catabolic enzyme is cytosolic N1-acetyltransferase (SSAT), which acetylates both SPM and SPD. The acetylated polyamines then move into the peroxisome where they are oxidised by polyamine oxidase. SSAT is necessary for the formation of PUT from SPD. SPM can also be back-converted into SPD by spermine oxidase in the cytoplasm (Minois, Carmona-Gutierrez, & Madeo, 2011). Polyamine transport plays an essential role in PA regulation. Despite substantial research, no polyamine transporter has been identified in mammals until now. Alternatively, it is thought that PAs uptake in mammals could be performed by endocytosis (Minois et al., 2011). 3. Biological roles in man

Fig. 1. Formulae of polyamines.

PUT, SPD and SPM, under physiological conditions, are strong flexible polycations exhibiting 2, 3 or 4 positive charges, respectively (see Fig. 1). They are able to interact with negatively charged macromolecules such as nucleic acids, phospholipids and proteins. These ionic interactions, which are reversible, lead to the stabilisation of DNA, RNA, membranes and some proteins (SánchezJiménez, Ruiz-Pérez, Urdiales, & Medina, 2013). This determines PAs as the essential factors for the growth, maintenance and function of normal cells.

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Polyamines participate in numerous physiological processes both favourable and injurious for human health. The knowledge of these various roles has been expanding greatly. 3.1. Participation in tumour growth Polyamines do not trigger cancer, but accelerate tumour growth. Enhanced levels of PAs biosynthesis in cancer tissues arises from the increased activity of enzymes responsible for their synthesis. In addition to the de novo synthesis, cells can uptake PAs from extracellular sources, such as cancer tissues, food, and intestinal microbiota. The increased polyamine availability enhances cell growth. Cancer cells with a greater capability to synthesise PAs are associated with increased production of proteinases, which can degrade surrounding tissues. Immune cells in an environment with increased PAs level, lose antitumour immune functions. The capability of cancer cells to invade and metastasise to new tissues is thus enhanced (Soda, 2011). Extracellular PAs are taken up into cancer cells via the polyamine transport system, an energy-dependent process that is upregulated in cancer cells. Deprivation of exogenous polyamines therefore started as a treatment approach in the 1990’s. The reduction of dietary PAs intake and partial intestinal decontamination showed (in preliminary clinical trials with prostate carcinoma patients) a well-observed and tolerated therapeutic regimen (Cipolla, Havouis, & Moulinoux, 2007). Some components of diet, particularly flavonoids, polyphenols and probiotics, were reported to reduce hyperproliferative role of PAs in colorectal cancer. 3.2. Effects on intestinal tract Dietary PAs, particularly SPM, contribute significantly to the intestinal polyamine pool and they are essential growth factors for small intestinal and colonic mucosal growth, maturation and regeneration. A great deal of this physiological research has been carried out with laboratory animals. Maturation of the suckling rat intestine by polyamines was recently reviewed by Dandrifosse (2009b). Considerable polyamine levels were observed in the lumen of human gut during the fasting state, which suggests endogenous secretion. A proximal absorption is supposed, due to significantly higher polyamine content found in the jejunum rather than in the ileum. Dietary PAs are almost completely absorbed in the small intestine. The proportion of the PAs, which may affect the large intestinal mucosal tissue, is primarily of microbial rather than of dietary origin. Initial studies deal with the ability of various microbiota species of human intestine to produce polyamines (Matsumoto & Benno, 2007). 3.3. Antioxidant activity Polyamine antioxidant activity seems to participate in the reduction of cell membranes and DNA damage. PAs at physiological concentrations are potent scavangers of hydroxyl radicals. SPD and SPM can also quench both singlet oxygen and hydrogen peroxide. Nevertheless, SPD and SPM can act as pro-oxidants and enhance oxidative damage to DNA components in the presence of free iron ions and hydrogen peroxide (Mozdzan, Szemraj, Rysz, Stolarek, & Nowak, 2006). Polyamine antioxidant and/or lysosomal stabilisation properties apparently cause anti-inflammatory activity in acute and chronic inflammation (Lagishetty & Naik, 2008). 3.4. Further effects PAs are involved in events inherent to genetically programmed cell death. Numerous links were identified between the

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polyamines and apoptic pathways, however, a lot of unresolved questions have endured (Seiler & Raul, 2005). SPM, SPD and PUT are essential to male and female reproductive processes and to embryo/fetal development. The mechanisms by which PAs regulate these multiple and diverse processes are not yet well explored (Lefèvre, Palin, & Murphy, 2011). As reviewed by Minois et al. (2011), recent level of understanding on the role of polyamine in ageing, suggests that PAs, particularly SPD, can be beneficial in healthy organisms but they may be harmful when disease appears. PAs are also implicated in bone growth and development. Tjabringa et al. (2008) observed that SPM regulates differentiation of adipose tissue-derived mesenchymal stem cells along the osteogenic lineage. Etiology and pathology of mental disorders, namely schizophrenia, mood disorders, anxiety and suicidal behaviour, are another field of the polyamine research. Uptake of SPD increases in Parkinson’s disease. Fiori and Turecki (2008) drew a conclusion that the polyamine pathway represents an important frontier for the development of neuropharmacological treatments. A review by Rhee, Kim, and Lee (2007) concluded that the polyamines could function as primordial stress molecules from bacteria to mammals, and might play an essential role in regulation of pathogen–host interactions. The polyamines, especially SPM, play an important role in allergy prevention in children, mainly by the regulation of food-allergen uptake by the intestine. They affect both innate and acquired immunity (Dandrifosse & Dandrifosse, 2009). 3.5. Toxicity and health risks Oral acute toxicity of the individual polyamines, determined in Wistar rats, was observed to be 2000, 600 and 600 mg kg1 body weight for PUT, SPD and SPM, respectively. The respective no-observed-adverse-effect levels (NOAEL) were 180, 83 and 19 mg kg1 body weight (Til, Falke, Prinsen, & Willems, 1997). Such extreme intakes of dietary PAs cannot be supposed, however, some of the polyamine catabolic by-products, particularly hydrogen peroxide, acrolein, 3-aminopropanal, 3-acetamidopropanal and 4-aminobutanal, may contribute to the etiology of several pathological states, such as cancer, neurodegenerative diseases, stroke and renal failure (for a review see Pegg, 2013). SPD or PUT can react under acidic conditions with nitrous acid forming N-nitrosopyrrolidine (NPYR), classified as a possible carcinogen. Pyrrolidin is formed from PUT after its deamination and cyclisation. NPYR can be then produced by the reaction of pyrrolidine with a nitrosating agent, particularly nitrites. NPYR is rarely found in heated cured lean pork. However, SPD was found to increase formation of N-nitrosodimethylamine, a probable carcinogen. Excessive SPM is cytotoxic to retinal pigment epithelial cells and can be involved in the mechanism of their degeneration (Kaneko et al., 2007). 3.6. Levels in human blood Polyamine levels in human blood is considered as an index of cell proliferation. Results from data collected by Ducros et al. (2009), show that usual concentrations are 8–14 and 5–8 nmol ml1 of packed red blood cells for SPD and SPM, respectively. Significantly higher levels of PAs in total blood, in a group of very old healthy individuals (96.5 ± 4.6 years) compared to younger groups (means 44.6 and 68.7 years) confirm previous reports on the role of PAs in determining human longevity (Pucciarelli et al., 2012).

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Different results were reported on the polyamine level changes in the blood of volunteers following one-short or long-term consumption of dietary polyamines. While polyamines contained in orange juice did not significantly affect the polyamine levels in blood up to 3 h after ingestion (Acheampong, MacLeod, & Wallace, 2009), daily intake of the polyamine-rich fermented soybean product natto for two months increased blood polyamine levels by a factor of 1.39 (Soda et al., 2009).

4. Polyamines in food Terms low, high and very high content, or level, will be used for

Health effects and occurrence of dietary polyamines: a review for the period 2005-mid 2013.

This review continues a previous one (Kalač & Krausová, 2005). Dietary polyamines spermidine and spermine participate in an array of physiological rol...
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