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1.  Biogenic Amines Degradation by Lactobacillus plantarum: Toward a Potential Application in Wine 
Biogenic amines (BA) in wine represent a toxicological risk for the health of the consumer, with several trade implications. In this study 26 strains of Lactobacillus plantarum were analyzed for their ability to degrade BA commonly found during wine fermentation. Two strains of L. plantarum were selected in reason of their ability to degrade putrescine and tyramine. The degradation was assessed in vitro, both in presence of the BA and in presence of the specific chemical precursor and of producer bacteria. The two L. plantarum biotypes were found capable to work synergically. In addition, the survival in wine-like medium and the aptitude to degrade malic acid after alcoholic fermentation of the selected L. plantarum strains was analyzed. Our results suggest the potential application of wine L. plantarum strains to design malolactic starter cultures able to degrade BA in wine.
doi:10.3389/fmicb.2012.00122
PMCID: PMC3316997  PMID: 22485114
lactic acid bacteria; amine degradation; biogenic amines; malolactic fermentation; wine; Lactobacillus plantarum; putrescine; tyramine
2.  Managing Your Wine Fermentation to Reduce the Risk of Biogenic Amine Formation 
Biogenic amines are nitrogenous organic compounds produced in wine from amino acid precursors mainly by microbial decarboxylation. The concentration of biogenic amines that can potentially be produced is dependent on the amount of amino acid precursors in the medium, the presence of decarboxylase positive microorganisms and conditions that enable microbial or biochemical activity such as the addition of nutrients to support the inoculated starter cultures for alcoholic and malolactic fermentation (MLF). MLF can be conducted using co-inoculation or an inoculation after the completion of alcoholic fermentation that may also affect the level of biogenic amines in wine. This study focused on the impact of the addition of complex commercial yeast and bacterial nutrients and the use of different MLF inoculation scenarios on the production of biogenic amines in wine. Results showed that the addition of complex nutrients to real grape must could potentially increase histamine concentrations in wine. The same experiment in synthetic grape must showed a similar trend for putrescine and cadaverine. The effect of different MLF inoculation scenarios was examined in two cultivars, Pinotage and Shiraz. Conflicting results was obtained. In the Shiraz, co-inoculation resulted in lower biogenic amine concentrations after MLF compared to before MLF, while the concentration was higher in the Pinotage. However, the production of biogenic amines was affected more by the presence of decarboxylase positive lactic acid bacteria than by the addition of complex nutrients or the inoculation scenario.
doi:10.3389/fmicb.2012.00076
PMCID: PMC3301445  PMID: 22419915
biogenic amines; nutrients; co-inoculation; malolactic fermentation; lactic acid bacteria; wine
3.  Three-Component Lysine/Ornithine Decarboxylation System in Lactobacillus saerimneri 30a 
Journal of Bacteriology  2013;195(6):1249-1254.
Lactic acid bacteria play a pivotal role in many food fermentations and sometimes represent a health threat due to the ability of some strains to produce biogenic amines that accumulate in foods and cause trouble following ingestion. These strains carry specific enzymatic systems catalyzing the uptake of amino acid precursors (e.g., ornithine and lysine), the decarboxylation inside the cell, and the release of the resulting biogenic amines (e.g., putrescine and cadaverine). This study aimed to identify the system involved in production of cadaverine from lysine, which has not been described to date for lactic acid bacteria. Strain Lactobacillus saerimneri 30a (formerly called Lactobacillus sp. 30a) produces both putrescine and cadaverine. The sequencing of its genome showed that the previously described ornithine decarboxylase gene was not associated with the gene encoding an ornithine/putrescine exchanger as in other bacteria. A new hypothetical decarboxylation system was detected in the proximity of the ornithine decarboxylase gene. It consisted of two genes encoding a putative decarboxylase sharing sequence similarities with ornithine decarboxylases and a putative amino acid transporter resembling the ornithine/putrescine exchangers. The two decarboxylases were produced in Escherichia coli, purified, and characterized in vitro, whereas the transporter was heterologously expressed in Lactococcus lactis and functionally characterized in vivo. The overall data led to the conclusion that the two decarboxylases and the transporter form a three-component decarboxylation system, with the new decarboxylase being a specific lysine decarboxylase and the transporter catalyzing both lysine/cadaverine and ornithine/putrescine exchange. To our knowledge, this is an unprecedented observation of a bacterial three-component decarboxylation system.
doi:10.1128/JB.02070-12
PMCID: PMC3592000  PMID: 23316036
4.  Tyramine biosynthesis in Enterococcus durans is transcriptionally regulated by the extracellular pH and tyrosine concentration 
Microbial biotechnology  2009;2(6):625-633.
Summary
The microbial decarboxylation of some amino acids leads to the undesirable presence of biogenic amines in foods. One of the most abundant and frequent biogenic amines found in fermented foods is tyramine, which is produced by the decarboxylation of tyrosine. In the present work, transcriptional analysis of tyramine biosynthesis in Enterococcus durans IPLA655, a strain isolated from cheese, was studied. The gene coding for the tyrosine decarboxylase (tdcA) and that coding for the tyrosine‐tyramine antiporter (tyrP) form an operon transcribed from the promoter PtdcA, the expression of which is regulated by the extracellular pH and tyrosine concentration. Quantification of gene expression during the log phase of growth showed high concentrations of tyrosine and acidic pH conditions to induce tdcA‐tyrP polycistronic messenger transcription.
doi:10.1111/j.1751-7915.2009.00117.x
PMCID: PMC3815318  PMID: 21255297
5.  Evidence of Two Functionally Distinct Ornithine Decarboxylation Systems in Lactic Acid Bacteria 
Biogenic amines are low-molecular-weight organic bases whose presence in food can result in health problems. The biosynthesis of biogenic amines in fermented foods mostly proceeds through amino acid decarboxylation carried out by lactic acid bacteria (LAB), but not all systems leading to biogenic amine production by LAB have been thoroughly characterized. Here, putative ornithine decarboxylation pathways consisting of a putative ornithine decarboxylase and an amino acid transporter were identified in LAB by strain collection screening and database searches. The decarboxylases were produced in heterologous hosts and purified and characterized in vitro, whereas transporters were heterologously expressed in Lactococcus lactis and functionally characterized in vivo. Amino acid decarboxylation by whole cells of the original hosts was determined as well. We concluded that two distinct types of ornithine decarboxylation systems exist in LAB. One is composed of an ornithine decarboxylase coupled to an ornithine/putrescine transmembrane exchanger. Their combined activities results in the extracellular release of putrescine. This typical amino acid decarboxylation system is present in only a few LAB strains and may contribute to metabolic energy production and/or pH homeostasis. The second system is widespread among LAB. It is composed of a decarboxylase active on ornithine and l-2,4-diaminobutyric acid (DABA) and a transporter that mediates unidirectional transport of ornithine into the cytoplasm. Diamines that result from this second system are retained within the cytosol.
doi:10.1128/AEM.07161-11
PMCID: PMC3298143  PMID: 22247134
6.  Control of Biogenic Amines in Food—Existing and Emerging Approaches 
Journal of Food Science  2010;75(7):R139-R150.
Biogenic amines have been reported in a variety of foods, such as fish, meat, cheese, vegetables, and wines. They are described as low molecular weight organic bases with aliphatic, aromatic, and heterocyclic structures. The most common biogenic amines found in foods are histamine, tyramine, cadaverine, 2-phenylethylamine, spermine, spermidine, putrescine, tryptamine, and agmatine. In addition octopamine and dopamine have been found in meat and meat products and fish. The formation of biogenic amines in food by the microbial decarboxylation of amino acids can result in consumers suffering allergic reactions, characterized by difficulty in breathing, itching, rash, vomiting, fever, and hypertension. Traditionally, biogenic amine formation in food has been prevented, primarily by limiting microbial growth through chilling and freezing. However, for many fishing based subsistence populations, such measures are not practical. Therefore, secondary control measures to prevent biogenic amine formation in foods or to reduce their levels once formed need to be considered as alternatives. Such approaches to limit microbial growth may include hydrostatic pressures, irradiation, controlled atmosphere packaging, or the use of food additives. Histamine may potentially be degraded by the use of bacterial amine oxidase or amine-negative bacteria. Only some will be cost-effective and practical for use in subsistence populations.
doi:10.1111/j.1750-3841.2010.01774.x
PMCID: PMC2995314  PMID: 21535566
biogenic amines; food additives; high hydrostatic pressure (HHP); irradiation; packaging; scombroid poisoning; starter cultures; temperature
7.  Factors Influencing Biogenic Amines Accumulation in Dairy Products 
Fermented foods are among the food products more often complained of having caused episodes of biogenic amines (BA) poisoning. Concerning milk-based fermented foods, cheese is the main product likely to contain potentially harmful levels of BA, specially tyramine, histamine, and putrescine. Prompted by the increasing awareness of the risks related to dietary uptake of high biogenic amine loads, in this review we report all those elaboration and processing technological aspects affecting BA biosynthesis and accumulation in dairy foods. Improved knowledge of the factors involved in the synthesis and accumulation of BA should lead to a reduction in their incidence in milk products. Synthesis of BA is possible only when three conditions converge: (i) availability of the substrate amino acids; (ii) presence of microorganisms with the appropriate catabolic pathway activated; and (iii) environmental conditions favorable to the decarboxylation activity. These conditions depend on several factors such as milk treatment (pasteurization), use of starter cultures, NaCl concentration, time, and temperature of ripening and preservation, pH, temperature, or post-ripening technological processes, which will be discussed in this chapter.
doi:10.3389/fmicb.2012.00180
PMCID: PMC3390585  PMID: 22783233
biogenic amines; cheese; producing microorganisms; pasteurization; starters; ripening; chemico-physical factors
8.  Biogenic amine production by the wine Lactobacillus brevis IOEB 9809 in systems that partially mimic the gastrointestinal tract stress 
BMC Microbiology  2012;12:247.
Background
Ingestion of fermented foods containing high levels of biogenic amines (BA) can be deleterious to human health. Less obvious is the threat posed by BA producing organisms contained within the food which, in principle, could form BA after ingestion even if the food product itself does not initially contain high BA levels. In this work we have investigated the production of tyramine and putrescine by Lactobacillus brevis IOEB 9809, of wine origin, under simulated gastrointestinal tract (GIT) conditions.
Results
An in vitro model that simulates the normal physiological conditions in the human digestive tract, as well as Caco-2 epithelial human cell lines, was used to challenge L. brevis IOEB 9809, which produced both tyramine and putrescine under all conditions tested. In the presence of BA precursors and under mild gastric stress, a correlation between enhancement of bacterial survival and a synchronous transcriptional activation of the tyramine and putrescine biosynthetic pathways was detected. High levels of both BA were observed after exposure of the bacterium to Caco-2 cells.
Conclusions
L. brevis IOEB 9809 can produce tyramine and putrescine under simulated human digestive tract conditions. The results indicate that BA production may be a mechanism that increases bacterial survival under gastric stress.
doi:10.1186/1471-2180-12-247
PMCID: PMC3499163  PMID: 23113922
Biogenic amines; Lactic acid bacteria; Putrescine; Tyramine; Food safety; Food toxicity
9.  Lactobacillus oligofermentans sp. nov., Associated with Spoilage of Modified-Atmosphere-Packaged Poultry Products 
Unidentified lactic acid bacterium (LAB) isolates which had mainly been detected in spoiled, marinated, modified atmosphere packaged (MAP) broiler meat products during two previous studies, were identified and analyzed for their phenotypic properties and the capability to produce biogenic amines. To establish the taxonomic position of these isolates, 16S rRNA gene sequence analysis, numerical analysis of ribopatterns, and DNA-DNA hybridization experiments were done. Unexpectedly for a meat-spoilage-associated LAB, the strains utilized glucose very weakly. According to the API 50 CHL test, arabinose and xylose were the only carbohydrates strongly fermented. None of the six strains tested for production of histamine, tyramine, tryptamine, phenylethylamine, putrescine, and cadaverine were able to produce these main meat-associated biogenic amines in vitro. The polyphasic taxonomy approach showed that these strains represent a new Lactobacillus species. The six isolates sequenced for the 16S rRNA encoding genes shared the highest similarity (95.0 to 96.3%) with the sequence of the Lactobacillus durianis type strain. In the phylogenetic tree, these isolates formed a distinct cluster within the Lactobacillus reuteri group, which also includes L. durianis. Numerical analyses of HindIII-EcoRI ribotypes placed all isolates together in a cluster with seven subclusters well separated from the L. reuteri group reference strains. The DNA-DNA hybridization levels between Lactobacillus sp. nov. isolates varied from 67 to 96%, and low hybridization levels (3 to 15%) were obtained with the L. durianis type strain confirming that these isolates belong to the same species different from L. durianis. The name Lactobacillus oligofermentans sp. nov. is proposed, with strain LMG 22743T (also known as DSM 15707T or AMKR18T) as the type strain.
doi:10.1128/AEM.71.8.4400-4406.2005
PMCID: PMC1183308  PMID: 16085830
10.  Genome Sequence of Lactobacillus saerimneri 30a (Formerly Lactobacillus sp. Strain 30a), a Reference Lactic Acid Bacterium Strain Producing Biogenic Amines 
Genome Announcements  2013;1(1):e00097-12.
Lactobacillus sp. strain 30a (Lactobacillus saerimneri) produces the biogenic amines histamine, putrescine, and cadaverine by decarboxylating their amino acid precursors. We report its draft genome sequence (1,634,278 bases, 42.6% G+C content) and the principal findings from its annotation, which might shed light onto the enzymatic machineries that are involved in its production of biogenic amines.
doi:10.1128/genomeA.00097-12
PMCID: PMC3569274  PMID: 23405290
11.  The influences of fish infusion broth on the biogenic amines formation by lactic acid bacteria 
Brazilian Journal of Microbiology  2013;44(2):407-413.
The influences of fish infusion decarboxylase broth (IDB) on biogenic amines (BA) formation by lactic acid bacteria (LAB) were investigated. BA productions by single LAB strains were tested in five different fish (anchovy, mackerel, white shark, sardine and gilthead seabream) IDB. The result of the study showed that significant differences in ammonia (AMN) and BA production were observed among the LAB strains in fish IDB (p < 0.05). The highest AMN and TMA production by LAB strains were observed for white shark IDB. The all tested bacteria had decarboxylation activity in fish IDB. The uppermost accumulated amines by LAB strains were tyramine (TYM), dopamine, serotonin and spermidine. The maximum histamine production was observed in sardine (101.69 mg/L) and mackerel (100.84 mg/L) IDB by Leuconostoc mesenteroides subsp. cremoris and Pediococcus acidophilus, respectively. Lactobacillus delbrueckii subsp. lactis and Pediococcus acidophilus had a high TYM producing capability (2943 mg/L and 1157 mg/L) in sardine IDB.
doi:10.1590/S1517-83822013000200010
PMCID: PMC3833135  PMID: 24294229
biogenic amines; lactic acid bacteria; starter cultures; fish infusion broth
12.  Lactic acid bacteria in Hamei and Marcha of North East India 
Indian Journal of Microbiology  2007;47(2):119-125.
Hamei and Marcha are mixed dough inocula used as starters for preparation of various indigenous alcoholic beverages in Manipur and Sikkim in India, respectively. These starters are traditionally prepared from rice with wild herbs and spices. Samples of Hamei and Marcha, collected from Manipur and Sikkim, respectively, were analysed for lactic acid bacterial composition. The population of lactic acid bacteria (LAB) was 6.9 and 7.1 Log cfu/g in Hamei and Marcha, respectively. On the basis of phenotypic and genotypic characters, LAB strains isolated from Hamei and Marcha were identified as Pediococcus pentosaceus, Lactobacillus plantarum and Lactobacillus brevis. Technological properties of LAB such as antimicrobial properties, effect on acidification, ability to produce biogenic amines and ethanol, degree of hydrophobicity and enzymatic activities were also performed. Pediococcus pentosaceus HS: B1, isolated from Hamei, was found to produce bacteriocin. None of the strains produced biogenic amines. LAB strains showed a strong acidifying ability and they also produced a wide spectrum of enzymes.
doi:10.1007/s12088-007-0024-8
PMCID: PMC3450109  PMID: 23100653
LAB; Hamei; Marcha
13.  Control of Biogenic Amines in Fermented Sausages: Role of Starter Cultures 
Biogenic amines show biological activity and exert undesirable physiological effects when absorbed at high concentrations. Biogenic amines are mainly formed by microbial decarboxylation of amino acids and thus are usually present in a wide range of foods, fermented sausages being one of the major biogenic amine sources. The use of selected starter cultures is one of the best technological measures to control aminogenesis during meat fermentation. Although with variable effectiveness, several works show the ability of some starters to render biogenic amine-free sausages. In this paper, the effect of different starter culture is reviewed and the factors determining their performance discussed.
doi:10.3389/fmicb.2012.00169
PMCID: PMC3345612  PMID: 22586423
starter cultures; biogenic amines; amino acid decarboxylase; fermented sausages; amino oxidase; autochthonous
14.  Initial catabolism of aromatic biogenic amines by Pseudomonas aeruginosa PAO: pathway description, mapping of mutations, and cloning of essential genes. 
Journal of Bacteriology  1987;169(6):2398-2404.
Pseudomonas aeruginosa PAO1 was able to utilize several aromatic biogenic amines as sole sources of carbon or nitrogen. These included the phenethylamines tyramine and dopamine and the phenethanolamines octopamine, synephrine, and norepinephrine. Initial catabolism of the phenethylamines was mediated by a membrane-bound tyramine dehydrogenase which produced 4-hydroxyphenylacetaldehyde (4HPAL) with tyramine as the substrate. The enzyme was induced by growth with both classes of amines. Initial catabolism of octopamine (except when present as the sole source of carbon and nitrogen) was mediated by a soluble enzyme with activity against the phenethanolamines but not against tyramine or dopamine. The product of the reaction with octopamine as substrate was also 4HPAL. Addition of NAD to reaction mixtures yielded 4-hydroxyphenylacetic acid and NADH. These activities, octopamine hydrolyase and 4-HPAL dehydrogenase (measured as a combined activity, OCAH-4HPALDH), were only induced by growth with phenethanolamines. However, the combined activities were not observed in extracts from cells grown with octopamine as the sole source of carbon and nitrogen, suggesting that an alternate pathway is used under this growth condition. Two independently isolated mutant strains were unable to utilize tyramine as a sole source of carbon or nitrogen. These mutants were also unable to utilize dopamine but grew at wild-type rates on the phenethanolamines. The mutations were mapped at about 70 min on the PAO1 chromosome with the chromosome-mobilizing plasmid R68.45, and both were linked to the catA1, mtu-9002, tyu-9009, and puuE mutations. DNA complementing both of the mutations was cloned on a single BamHI fragment approximately 13.8 kilobase pairs in length. Analysis of a subcloned fragment showed that the two mutations were in different genes.
PMCID: PMC212074  PMID: 3034855
15.  Naturally Occurring Toxic Factors in Plants and Animals Used as Food 
Toxic components of natural foodstuffs are discussed, with special reference to lathyrogens, pressor amines, azoxyglycosides, and labile sulfur compounds. The osteolathyrogen, γ-glutamyl-β-aminopropionitrile, in sweet pea (Lathyrus odoratus) seeds induces skeletal deformities and aortic rupture, probably by interfering with normal maturation of collagen fibres. Neurolathyrism in man may be caused by β-N-oxalyl-L-α,β-diaminopropionic acid, a neurotoxin recently identified in Lathyrus sativus seeds. Histamine, tyramine, noradrenaline, serotonin and other pressor amines occur in fruits and fermented foods such as bananas, pineapples, cheese and wine. Consumption of such foods by patients taking monoamine oxidase-inhibiting drugs (e.g. tranylcypromine) may produce serious hypertensive crises. Cycad nuts, widely used as human food in tropical and subtropical areas, contain a potent carcinogen, methyl azoxymethanol, which is more or less removed prior to use by leaching in water. Consumption of plants of the onion, cabbage and cress families introduces into the body such toxic chemicals as benzyl cyanide, goitrin and thiocyanates. The lachrymatory substance in onions is propenyl sulfenic acid.
PMCID: PMC1935363  PMID: 5905948
16.  Sequencing and Transcriptional Analysis of the Biosynthesis Gene Cluster of Putrescine-Producing Lactococcus lactis ▿ †  
Applied and Environmental Microbiology  2011;77(18):6409-6418.
Lactococcus lactis is a prokaryotic microorganism with great importance as a culture starter and has become the model species among the lactic acid bacteria. The long and safe history of use of L. lactis in dairy fermentations has resulted in the classification of this species as GRAS (General Regarded As Safe) or QPS (Qualified Presumption of Safety). However, our group has identified several strains of L. lactis subsp. lactis and L. lactis subsp. cremoris that are able to produce putrescine from agmatine via the agmatine deiminase (AGDI) pathway. Putrescine is a biogenic amine that confers undesirable flavor characteristics and may even have toxic effects. The AGDI cluster of L. lactis is composed of a putative regulatory gene, aguR, followed by the genes (aguB, aguD, aguA, and aguC) encoding the catabolic enzymes. These genes are transcribed as an operon that is induced in the presence of agmatine. In some strains, an insertion (IS) element interrupts the transcription of the cluster, which results in a non-putrescine-producing phenotype. Based on this knowledge, a PCR-based test was developed in order to differentiate nonproducing L. lactis strains from those with a functional AGDI cluster. The analysis of the AGDI cluster and their flanking regions revealed that the capacity to produce putrescine via the AGDI pathway could be a specific characteristic that was lost during the adaptation to the milk environment by a process of reductive genome evolution.
doi:10.1128/AEM.05507-11
PMCID: PMC3187148  PMID: 21803900
17.  BIOGENIC AMINES IN CULTURED NEUROBLASTOMA AND ASTROCYTOMA CELLS 
The Journal of Cell Biology  1974;63(1):64-70.
The presence of biogenic amines in cultured cells of mouse neuroblastoma C-1300 (clone NB-2a) was suggested by fluorescence-microscope histochemistry. Incubation in media containing L-[14C]tyrosine and L-[14C]tryptophan for 24 h, followed by high-voltage electrophoresis, radiochromatogram scanning, and scintillation counting, confirmed the presence of [14C]dopamine, [14C]norepinephrine, [14C]epinephrine, [14C]serotonin, [14C]tyramine, and [14C]octopamine. Dopamine, norepinephrine, epinephrine, and serotonin were demonstrated spectrophotofluorometrically in concentrations, expressed as micrograms amine per milligram protein, of 1.19, 0.027, 0.038, and 0.148, respectively, for cells in a stationary growth phase. Fluorescence-microscope histochemistry also suggested the presence of biogenic amines in cultured astrocytoma cells (cell line C6). Spectrophotofluorometric assay of cells in a stationary growth phase demonstrated intracellular dopamine, norepinephrine, epinephrine, and serotonin in concentrations significantly lower than those of neuroblastoma cells.
PMCID: PMC2109339  PMID: 4370924
18.  Reducing Biogenic-Amine-Producing Bacteria, Decarboxylase Activity, and Biogenic Amines in Raw Milk Cheese by High-Pressure Treatments 
Biogenic amines may reach concentrations of public health concern in some cheeses. To minimize biogenic amine buildup in raw milk cheese, high-pressure treatments of 400 or 600 MPa for 5 min were applied on days 21 and 35 of ripening. On day 60, counts of lactic acid bacteria, enterococci, and lactobacilli were 1 to 2 log units lower in cheeses treated at 400 MPa and 4 to 6 log units lower in cheeses treated at 600 MPa than in control cheese. At that time, aminopeptidase activity was 16 to 75% lower in cheeses treated at 400 MPa and 56 to 81% lower in cheeses treated at 600 MPa than in control cheese, while the total free amino acid concentration was 35 to 53% higher in cheeses treated at 400 MPa and 3 to 15% higher in cheeses treated at 600 MPa, and decarboxylase activity was 86 to 96% lower in cheeses treated at 400 MPa and 93 to 100% lower in cheeses treated at 600 MPa. Tyramine, putrescine, and cadaverine were the most abundant amines in control cheese. The total biogenic amine concentration on day 60, which reached a maximum of 1.089 mg/g dry matter in control cheese, was 27 to 33% lower in cheeses treated at 400 MPa and 40 to 65% lower in cheeses treated at 600 MPa. On day 240, total biogenic amines attained a concentration of 3.690 mg/g dry matter in control cheese and contents 11 to 45% lower in cheeses treated at 400 MPa and 73 to 76% lower in cheeses treated at 600 MPa. Over 80% of the histidine and 95% of the tyrosine had been converted into histamine and tyramine in control cheese by day 60. Substrate depletion played an important role in the rate of biogenic amine buildup, becoming a limiting factor in the case of some amino acids.
doi:10.1128/AEM.03368-12
PMCID: PMC3568586  PMID: 23241980
19.  Microcolumn Separation of Amine Metabolites in the Fruit Fly 
Analytical chemistry  2005;77(16):5349-5355.
Electrophoretic resolution of fourteen biogenic amines and metabolites with similar mobilities is addressed by employing micellar electrokinetic capillary chromatography coupled to amperometric electrochemical detection. The present study describes the optimization of separation conditions to achieve resolution of analytes of biological significance within 20 minutes in a single separation. They include dopamine, epinephrine, norepinephrine, octopamine (OA), l-3, 4-dihydroxyphenylalanine, tyramine (TA), and serotonin as well as metabolites 5-hydroxyindolacetic acid, 3,4-dihydroxyphenylacetic acid, homovanillic acid, and 3-methoxytyramine in addition to N-acetylated metabolites including N-acetyl dopamine, N-acetyl octopamine (naOA), and N-acetyl serotonin. The optimized conditions used result in excellent reproducibility and predictable peak shifting, thus enabling identification of several metabolites along with their biogenic amine precursors in biological samples, specifically from the fruit fly Drosophila melanogaster. The separation method is sensitive, selective and quantitative as demonstrated by its capacity to detect changes in TA, OA, and naOA present in the head homogenates of the Canton-S and mutant inactive1 Drosophila lines. Quantitative analysis of metabolites in conjunction with their biogenic amine precursors in a single separation offers tremendous potential to understand the physiological processes and underlying mechanisms mediated by various biogenic amines in Drosophila and other animals.
doi:10.1021/ac050474m
PMCID: PMC1351352  PMID: 16097779
20.  Chemical Characterization of Wines Fermented with Various Malo-lactic Bacteria1 
Applied Microbiology  1966;14(4):608-615.
Six malo-lactic strains of lactic acid bacteria were isolated from California wines and identified as Lactobacillus delbrueckii, L. buchneri, L. brevis, Leuconostoc citrovorum, and two strains of Pediococcus cerevisiae. Malo-lactic fermentation was induced in separate lots of wine by inoculation of each lot with one of the strains of bacteria. Malo-lactic fermentation had occurred in each inoculated wine within 2 months. The resultant wines were subjected to chemical analysis, including gas chromatographic examination of concentrated extracts of the wines. Only a few differences in composition were found when the malo-lactic wines were compared one with another. The differences that were found were in volatile acidity and in concentrations of acetoin (plus diacetyl) and probably diethyl succinate.
PMCID: PMC546795  PMID: 5927037
21.  Origin of the Putrescine-Producing Ability of the Coagulase-Negative Bacterium Staphylococcus epidermidis 2015B▿  
Applied and Environmental Microbiology  2010;76(16):5570-5576.
A multiplex PCR method, aimed at the detection of genes associated with biogenic amine production, identified the odc gene encoding ornithine decarboxylase in 1 of 15 strains of Staphylococcus epidermidis. The ability of the positive strain, S. epidermidis 2015B, to produce putrescine in vitro was demonstrated by high-performance liquid chromatography (HPLC). In this strain, the odc gene was detected on plasmid DNA, suggesting that the ability to form putrescine is carried by a mobile element, which explains the fact that the trait is strain dependent within the S. epidermidis species. A 6,292-bp nucleotide sequence harboring the putative odc gene was determined. S. epidermidis ornithine decarboxylase (ODC) showed 60 to 65% sequence identity with known ODCs of Gram-positive as well as Gram-negative bacteria. Downstream of the odc gene, a gene encoding a putative amino acid transporter was found that shared 59% sequence identity with the ornithine/putrescine exchanger (PotE) of Escherichia coli. Cloning and expression of the potE gene of S. epidermis 2015B in Lactococcus lactis demonstrated that the gene product transported ornithine and putrescine into the cells and efficiently exchanged putrescine for ornithine. Analysis of the flanking regions showed high identity levels with different S. epidermidis plasmid sequences, which would confirm the plasmidic location of the odc operon. It follows that the odc and potE gene pair encodes a putrescine-producing pathway in S. epidermis 2015B that was acquired through horizontal gene transfer.
doi:10.1128/AEM.00441-10
PMCID: PMC2918964  PMID: 20581187
22.  Effect of sucrose on the generation of free amino acids and biogenic amines in Chinese traditional dry-cured fish during processing and storage 
The Chinese traditional dry-cured grass carp fish (Layú) was processed with (A) and without (B) sucrose. Higher levels of free amino acids (FAA) and biogenic amines were detected in the final products when compared to the fresh fish. In the presence of sucrose, Layú A had higher total free amino acids (39.9 g/kg DW) but lower total biogenic amines (112.5 mg/kg DW) than those in Layú B (35.4 g/kg DW and 143.7 mg/kg DW, respectively) after ageing. After 60 days, the products storaged at 4 °C had lower amount biogenic amines (Layú A: 112.2~579.5; Layú B: 144~593.8 mg/kg DW) than those at 20 °C (Layú A: 112.2~974.8; Layú B: 144~773.4 mg/kg DW), indicating that low temperature storage was a safer procedure.
doi:10.1007/s13197-010-0130-1
PMCID: PMC3551093  PMID: 23572718
Layú; Dry-cured; Free amino acids; Biogenic amines; Sucrose
23.  Amine content of vaginal fluid from untreated and treated patients with nonspecific vaginitis. 
Journal of Clinical Investigation  1979;63(5):828-835.
We examined the vaginal washings from patients with nonspecific vaginitis (NSV) to seek biochemical markers and possible explanations for the signs and symptoms of this syndrome. Seven amines were identified including methylamine, isobutylamine, putrescine, cadaverine, histamine, tyramine, and phenethylamine. These amines may contribute to the symptoms of NSV and may contribute to the elevated pH of the vaginal discharge. They may also be partly responsible for the "fishy" odor that is characteristic of vaginal discharges from these patients. Among the seven amines, putrescine and cadaverine were the most abundant and were present in all vaginal discharges from each of ten patients before treatment. These amines are produced in vitro during growth of mixed vaginal bacteria in chemically defined medium, presumably by decarboxylation of the corresponding amino acids. We hypothesize the anaerobic vaginal organisms, previously shown to be quantitatively increased in NSV, are responsible for the amine production, because metronidazole inhibited the production of amines by vaginal bacteria in vitro, and Haemophilus vaginalis did not produce amines. H. vaginalis did release high concentrations of pyruvic acid and of amino acids during growth in peptone-starch-dextrose medium, whereas, other vaginal flora consumed both pyruvic acid and amino acids in the same medium during growth. These findings suggest that a symbiotic relationship may exist between H. vaginalis and other vaginal flora in patients with NSV.
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PMCID: PMC372023  PMID: 447831
24.  Aminergic Control and Modulation of Honeybee Behaviour 
Current Neuropharmacology  2006;4(4):259-276.
Biogenic amines are important messenger substances in the central nervous system and in peripheral organs of vertebrates and of invertebrates. The honeybee, Apis mellifera, is excellently suited to uncover the functions of biogenic amines in behaviour, because it has an extensive behavioural repertoire, with a number of biogenic amine receptors characterised in this insect.
In the honeybee, the biogenic amines dopamine, octopamine, serotonin and tyramine modulate neuronal functions in various ways. Dopamine and serotonin are present in high concentrations in the bee brain, whereas octopamine and tyramine are less abundant. Octopamine is a key molecule for the control of honeybee behaviour. It generally has an arousing effect and leads to higher sensitivity for sensory inputs, better learning performance and increased foraging behaviour. Tyramine has been suggested to act antagonistically to octopamine, but only few experimental data are available for this amine. Dopamine and serotonin often have antagonistic or inhibitory effects as compared to octopamine.
Biogenic amines bind to membrane receptors that primarily belong to the large gene-family of GTP-binding (G) protein coupled receptors. Receptor activation leads to transient changes in concentrations of intracellular second messengers such as cAMP, IP3 and/or Ca2+. Although several biogenic amine receptors from the honeybee have been cloned and characterised more recently, many genes still remain to be identified. The availability of the completely sequenced genome of Apis mellifera will contribute substantially to closing this gap.
In this review, we will discuss the present knowledge on how biogenic amines and their receptor-mediated cellular responses modulate different behaviours of honeybees including learning processes and division of labour.
PMCID: PMC2475800  PMID: 18654639
Serotonin; dopamine; octopamine; tyramine; honeybee; behaviour; division of labour; amine receptors
25.  Lactobacillus reuteri-Specific Immunoregulatory Gene rsiR Modulates Histamine Production and Immunomodulation by Lactobacillus reuteri 
Journal of Bacteriology  2013;195(24):5567-5576.
Human microbiome-derived strains of Lactobacillus reuteri potently suppress proinflammatory cytokines like human tumor necrosis factor (TNF) by converting the amino acid l-histidine to the biogenic amine histamine. Histamine suppresses mitogen-activated protein (MAP) kinase activation and cytokine production by signaling via histamine receptor type 2 (H2) on myeloid cells. Investigations of the gene expression profiles of immunomodulatory L. reuteri ATCC PTA 6475 highlighted numerous genes that were highly expressed during the stationary phase of growth, when TNF suppression is most potent. One such gene was found to be a regulator of genes involved in histidine-histamine metabolism by this probiotic species. During the course of these studies, this gene was renamed the Lactobacillus reuteri-specific immunoregulatory (rsiR) gene. The rsiR gene is essential for human TNF suppression by L. reuteri and expression of the histidine decarboxylase (hdc) gene cluster on the L. reuteri chromosome. Inactivation of rsiR resulted in diminished TNF suppression in vitro and reduced anti-inflammatory effects in vivo in a trinitrobenzene sulfonic acid (TNBS)-induced mouse model of acute colitis. A L. reuteri strain lacking an intact rsiR gene was unable to suppress colitis and resulted in greater concentrations of serum amyloid A (SAA) in the bloodstream of affected animals. The PhdcAB promoter region targeted by rsiR was defined by reporter gene experiments. These studies support the presence of a regulatory gene, rsiR, which modulates the expression of a gene cluster known to mediate immunoregulation by probiotics at the transcriptional level. These findings may point the way toward new strategies for controlling gene expression in probiotics by dietary interventions or microbiome manipulation.
doi:10.1128/JB.00261-13
PMCID: PMC3889603  PMID: 24123819

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