Abstract
With the only exception of glycine, all amino acids exist in two specular structures which are mirror images of each other, called D-(dextro) and L-(levo) enantiomers. During evolution, L-amino acids were preferred for protein synthesis and main metabolism; however, the D-amino acids (D-AAs) acquired different and specific functions in different organisms (from playing a structural role in the peptidoglycan of the bacterial cell wall to modulating neurotransmission in mammalian brain). With the advent of sophisticated and sensitive analytical techniques, it was established during the past few decades that many foods contain considerable amounts of D-AAs: we consume more than 100 mg of D-AAs every day. D-AAs are present in a variety of foodstuffs, where they fulfill a relevant role in producing differences in taste and flavor and in their antimicrobial and antiaging properties from the corresponding L-enantiomers. In this review, we report on the derivation of D-AAs in foods, mainly originating from the starting materials, fermentation processes, racemization during food processing, or contamination. We then focus on leading-edge methods to identify and quantify D-AAs in foods. Finally, current knowledge concerning the effect of D-AAs on the nutritional state and human health is summarized, highlighting some positive and negative effects. Notwithstanding recent progress in D-AA research, the relationships between presence and nutritional value of D-AAs in foods represent a main scientific issue with interesting economic impact in the near future.
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References
Abe H, Park JN, Fukumoto Y, Fujita E, Tanaka T, Washio T, Otsuka S, Shimizu T, Watanabe K (1999) Occurrence of D-amino acids in fish sauces and other fermented fish products. Fisheries Sci 65:637–641. https://doi.org/10.2331/fishsci.65.637
Albertini A, Mentasti T, Moretti VM, Bellagamba F, Luzzana U, Valfre F (1996) Occurrence of free D-amino acids in milk from food-producing animals. Milchwissenschaft 51:127–129
Aldag RW, Young JL, Yamamoto M (1971) An enzymic chromatographic procedure for the determination of D-amino acids in plant and soil extracts. Phytochemistry 10:267–274. https://doi.org/10.1016/S0031-9422(00)94039-1
Ali HS, Pätzold R, Brückner H (2010) Gas chromatographic determination of amino acid enantiomers in bottled and aged wines. Amino Acids 38:951–958. https://doi.org/10.1007/s00726-009-0304-1
Balagot RC, Ehrenpreis S, Kubota K, Greenberg J (1981) Analgesia in mice and humans by D-phenylalanine: relation to inhibition of enkephalin degradation and enkephalin levels. Pain 11:S21. https://doi.org/10.1016/0304-3959(81)90228-1
Bassoli A, Borgonovo G, Caremoli F, Mancuso G (2014) The taste of D- and L-amino acids: in vitro binding assays with cloned human bitter (TAS2Rs) and sweet (TAS1R2/TAS1R3) receptors. Food Chem 150:27–33
Bidlingmeyer BA, Cohen SA, Tarvin TL (1984) Rapid analysis of amino acids using pre-column derivatization. J Chromatogr 336:93–104. https://doi.org/10.1016/S0378-4347(00)85133-6
Brückner H, Fujii N (2010) D-amino acids in chemistry, life sciences, and biotechnology. Wiley-VCH, Weinheim
Brückner H, Hausch M (1989) Detection of free D-amino acids in food by chiral phase capillary gas chromatography. J High Res Chromatog 12:680–684. https://doi.org/10.1002/jhrc.1240121012
Brückner H, Hausch M (1990) D-amino acids in dairy products: detection, origin and nutritional aspects. I. Milk, fermented milk, fresh cheese and acid curd cheese. Milchwissenschaft 45:357–360
Brückner H, Westhauser T (1994) Chromatographic determination of D-amino acids as native constituents of vegetables and fruits. Chromatographia 39:419–426. https://doi.org/10.1007/BF02278756
Brückner H, Westhauser T (2003) Chromatographic determination of L- and D-amino acids in plants. Amino Acids 24:43–55. https://doi.org/10.1007/s00726-002-0322-8
Brückner H, Becker D, Lüpke M (1993) Chirality of amino acids of microorganisms used in food biotechnology. Chirality 5:385–392. https://doi.org/10.1002/chir.530050521
Brückner H, Westhauser T, Godel H (1995) Liquid chromatographic determination of D-and L-amino acids by derivatization with o-phthaldialdehyde and N-isobutyryl-L-cysteine. Applications with reference to the analysis of peptidic antibiotics, toxins, drugs and pharmaceutically used amino acids. J Chromatogr A 711:201–215. https://doi.org/10.1016/0021-9673(95)00158-j
Brückner H, Justus J, Kirschbaum J (2001) Saccharide induced racemization of amino acids in the course of the Maillard reaction. Amino Acids 21:429–433. https://doi.org/10.1007/s0072601700
Buck RH, Krummen K (1987) High-performance liquid chromatographic determination of enantiomeric amino acids and amino alcohols after derivatization with o-phthaldialdehyde and various chiral mercaptans: Application to peptide hydrolysates. J Chromatogr 387:255–265. https://doi.org/10.1016/S0021-9673(01)94529-7
Bunjapamai S, Mahoney RR, Fagerson IS (1982) Determination of D-amino acids in some processed foods and effect of racemization on in vitro digestibility of casein. J Food Sci 47:1229–1234. https://doi.org/10.1111/j.1365-2621.1982.tb07654.x
Carlavilla D, Moreno-Arribas MV, Fanali S, Cifuentes A (2006) Chiral MEKC-LIF of amino acids in foods: analysis of vinegars. Electrophoresis 27(13):2551–2557. https://doi.org/10.1002/elps.200500909
Casado FJ, Sánchez AH, Rejano L, Montaño A (2007) D-amino acid formation in sterilized alkali-treated olives. J Agric Food Chem 55:3503–3507. https://doi.org/10.1021/jf0701685
Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK (2011) Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J 30:3442–3453. https://doi.org/10.1038/emboj.2011.246
Chattopadhyay S, Raychaudhuri U, Chakraborty R (2014) Artificial sweeteners—a review. J Food Sci Technol 51:611–621. https://doi.org/10.1007/s13197-011-0571-1
Chen Z, Kondrashina A, Greco I, Gamon LF, Lund MN, Giblin L, Davies MJ (2019) Effects of protein-derived amino acid modification products present in infant formula on metabolic function, oxidative stress, and intestinal permeability in cell models. J Agric Food Chem 67:5634–5646. https://doi.org/10.1021/acs.jafc.9b01324
Chiavaro E, Caligiani A, Palla G (1998) Chiral indicators of ageing in balsamic vinegars of Modena. Int J Food Sci 10:329–337
Csapò J, Csapò-Kiss Z, Stefler J (1995) Influence of mastitis on D-amino acid content of milk. J Dairy Sci 78:2375–2381. https://doi.org/10.3168/jds.S0022-0302(95)76865-5
Csapò J, Varga-Visi E, Loki K, Albert CS, Salamon SZ (2008) The influence of extrusion on loss and racemization of amino acids. Amino Acids 34:287–292. https://doi.org/10.1007/s00726-006-0484-x
Csapó J, Albert CS, Csapó-Kiss ZS. (2009) The D-amino acid content of foodstuffs (a review). Acta Univ. Sapientiae, Alimentaria, 2, 1: 5–30
De Jonge BL, Gage D, Xu N (2002) The carboxyl terminus of peptidoglycan stem peptides is a determinant for methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 46:3151–3155. https://doi.org/10.1128/AAC.46.10.3151
Einarsson S, Josefsson B, Möller P, Sanchez D (1987) Separation of amino acid enantiomers and chiral amines using precolumn derivatization with (+)-1-(9-fluorenyl)ethyl chloroformate and reversed-phase liquid chromatography. Anal Chem 59:1191–1195. https://doi.org/10.1021/ac00135a025
Erbe T, Brückner H (2000) Chromatographic determination of amino acid enantiomers in beers and raw materials used for their manufacture. J Chromatogr A 881:81–91. https://doi.org/10.1016/s0021-9673(00)00255-7
Eto S, Yamaguchi M, Bounoshita M, Mizukoshi T, Miyano H (2011) High-throughput comprehensive analysis of D- and L-amino acids using ultra-high performance liquid chromatography with a circular dichroism (CD) detector and its application to food samples. J Chromatogr B Analyt Technol Biomed Life Sci. 879:3317–3325. https://doi.org/10.1016/j.jchromb.2011.07.025
Finley JW (1985) Environmental effects of protein quality. In: Chemical changes in food during processing. Inst. Food Technologists Basic Symp. Ser., AVI Publ. Westport Conn.. 443–482
Friedman M (1999) Chemistry, nutrition, and microbiology of D-amino acids. J Agr Food Chem 47:3457–3479. https://doi.org/10.1021/jf990080u
Friedman M (2007) Nutritional evaluation of D-amino acids. In: Konno R et al (eds) D-amino acids: a new frontier in amino acid and protein research. Nova Science Publishers, New York, pp 285–298
Friedman M, Levin CE (2012) Nutritional and medicinal aspects of D-amino acids. Amino Acids 42:1553–1582. https://doi.org/10.1007/s00726-011-0915-1
Friedman M, Liardon R (1985) Racemization kinetics of amino acid residues in alkali-treated soybean proteins. J Agric Food Chem 33:666–672. https://doi.org/10.1021/jf00064a025
Friedman M, Zahnley JC, Masters PM (1981) Relationship between in vitro digestibility of casein and its content of lysinoalanine and D-amino acids. J Food Sci 46:127–134. https://doi.org/10.1111/j.1365-2621.1981.tb14545.x
Fukuda M, Tokumura A, Ogawa T (1973) D-alanine in germinating Pisum sativum seedlings. Phytochem 12:2593–2595. https://doi.org/10.1016/0031-9422(73)85061-7
Gandolfi I, Palla G, Delprato L, Nisco F, Marchelli R, Salvadori C (1992) D-amino acids in milk as related to heat treatments and bacterial activity. J Food Sci 57:377–379. https://doi.org/10.1111/j.1365-2621.1992.tb05498.x
Gandolfi I, Palla G, Marchelli R, Dossena A, Puelli S, Salvadori C (1994) D-alanine in fruit juices: a molecular marker of bacterial activity, heat treatments and shelf-life. J Food Sci 59:152–154. https://doi.org/10.1111/j.1365-2621.1994.tb06921.x
Gatti R, Gioia MG, Leoni A, Andreani A (2010) 2,5-dimethyl-1H-pyrrole-3,4-dicarbaldehyde as a precolumn derivatization reagent for HPLC/UV detection of amino acids. J Pharm Biomed Anal 53:207–211. https://doi.org/10.1016/j.jpba.2009.12.031
Genchi G (2017) An overview on D-amino acids. Amino Acids 49:1521–1533. https://doi.org/10.1007/s00726-017-2459-5
Gilani GS, Cockell KA, Sepehr E (2005) Effects of antinutritional factors on protein digestibility and amino acid availability in foods. J AOAC Int 88:967–987
Gilani GS, Xiao CW, Cockell KA (2012) Impact of antinutritional factors in food proteins on the digestibility of protein and the bioavailability of amino acids and on protein quality. Br J Nutr 108:S315–S332. https://doi.org/10.1017/S0007114512002371
Gioia MG, Cacciari B, Leoni A, Gatti R (2006) 2,7-dimethyl-3,8-dinitrodipyrazolo[1,5-a:1′,5′-d]pyrazine-4,9-dione: a new labelling reagent for liquid chromatographic analysis of amino acids. Anal Chim Acta 579:152–157. https://doi.org/10.1016/j.aca.2006.07.035
Giuffrida A, León C, García-Cañas V, Cucinotta V, Cifuentes A (2009) Modified cyclodextrins for fast and sensitive chiral-capillary electrophoresis-mass spectrometry. Electrophoresis 30:1734–1742. https://doi.org/10.1002/elps.200800333
Gobbetti M, Simonetti MS, Rossi J, Cossignani L, Corsetti A, Damiani P (1994) Free D- and L-amino acid evolution during sourdough fermentation and baking. J Food Sci 59:881–884. https://doi.org/10.1111/j.1365-2621.1994.tb08149.x
Gogami Y, Okada K, Oikawa T (2011) High-performance liquid chromatography analysis of naturally occurring D-amino acids in sake. J Chromatogr B Analyt Technol Biomed Life Sci 879:3259–3267. https://doi.org/10.1016/j.jchromb.2011.04.006
Guillén-Casla V, León-González ME, Pérez-Arribas LV, Polo-Díez LM (2010) Direct chiral determination of free amino acid enantiomers by two-dimensional liquid chromatography: application to control transformations in E-beam irradiated foodstuffs. Anal Bioanal Chem 397:63–75. https://doi.org/10.1007/s00216-009-3376-6
Hamase K, Miyoshi Y, Ueno K, Han H, Hirano J, Morikawa A, Mita M, Kaneko T, Lindner W, Zaitsu K (2010) Simultaneous determination of hydrophilic amino acid enantiomers in mammalian tissues and physiological fluids applying a fully automated micro-two-dimensional high-performance liquid chromatographic concept. J Chromatogr A 1217:1056–1062. https://doi.org/10.1016/j.chroma.2009.09.002
Harada M, Karakawa S, Yamada N, Miyano H, Shimbo K (2019) Biaryl axially chiral derivatizing agent for simultaneous separation and sensitive detection of proteinogenic amino acid enantiomers using liquid chromatography-tandem mass spectrometry. J Chromatogr A 1593:91–101. https://doi.org/10.1016/j.chroma.2019.01.075
Hayase F, Kato H, Fujimaki M (1973) Racemization of amino acid residues in protein during roasting. Agric Biol Chem 37:191–192
Heresco-Levy U, Vass A, Bloch B, Wolosker H, Dumin E, Balan L, Deutsch L, Kremer I (2009) Pilot controlled trial of D-serine for the treatment of post-traumatic stress disorder. Int J Neuropsychopharmacol 12:1275–1282. https://doi.org/10.1017/S1461145709000339
Herrero M, Ibáñez E, Martín-Alvarez PJ, Cifuentes A (2007) Analysis of chiral amino acids in conventional and transgenic maize. Anal Chem 79:5071–5077. https://doi.org/10.1021/ac070454f
Horcajo P, de Pedro MA, Cava F (2012) Peptidoglycan plasticity in bacteria: stress-induced peptidoglycan editing by noncanonical D-amino acids. Microb Drug Resist 18:306–313. https://doi.org/10.1089/mdr.2012.0009
Ilisz I, Berkecz R, Péter A (2008) Application of chiral derivatizing agents in the high-performance liquid chromatographic separation of amino acid enantiomers: a review. J Pharm Biomed Anal 47:1–15. https://doi.org/10.1016/j.jpba.2007.12.013
Inaba Y, Mizukami K, Hamada-Sato N, Kobayashi T, Imada C, Watanabe E (2003) Development of a D-alanine sensor for the monitoring of a fermentation using the improved selectivity by the combination of D-amino acid oxidase and pyruvate oxidase. Biosens Bioelectron 19:423–431. https://doi.org/10.1016/S0956-5663(03)00200-8
Innocente N, Palla G (1999) Occurrence of D-amino acids in a typical semi-hard cheese. J Dairy Res 66:633–637. https://doi.org/10.1017/S0022029999003829
Ishida Y, Fujita T, Asai K (1981) New detection and separation method for amino acids by high-performance liquid chromatography. J Chromatogr 204:143–148. https://doi.org/10.1016/s0021-9673(00)81650-7
Jin D, Miyahara T, Oe T, Toyo'oka T (1999) Determination of D-amino acids labeled with fluorescent chiral reagents, R(−)- and S(+)-4-(3-isothiocyanatopyrrolidin-1-yl)-7-(N,N-dimethylaminosulfonyl)-2,1,3-benzoxadiazoles, in biological and food samples by liquid chromatography. Anal Biochem 269:124–132. https://doi.org/10.1006/abio.1998.3090
Kato M, Fukushima T, Santa T, Homma H, Imai K (1995) Determination of D-amino acids, derivatized with 4-fluoro-7-nitro-2, 1, 3-benzoxadiazole (NBD-F), in wine samples by high-performance liquid chromatography. Biomed Chromatogr 9:193–194. https://doi.org/10.1002/bmc.1130090409
Kato S, Ishihara T, Hemmi H, Kobayashi H, Yoshimura T (2011) Alterations in D-amino acid concentrations and microbial community structures during the fermentation of red and white wines. J Biosci Bioeng 111:104–108. https://doi.org/10.1016/j.jbiosc.2010.08.019
Kawasaki Y, Ogawa T, Sasaoka K (1982) Two pathways for formation of D-amino acid conjugates in pea seedlings. Agric Biol Chem 46:1–5. https://doi.org/10.1271/bbb1961.46.1
Kawase T, Furuse M (2019) Long-term administration of yoghurt improves spatial memory in mice. J Pet Anim Nutr 22(1):1–13
Konya Y, Taniguchi M, Fukusaki E (2017) Novel high-throughput and widely-targeted liquid chromatography-time of flight mass spectrometry method for D-amino acids in foods. J Biosci Bioeng 123:126–133. https://doi.org/10.1016/j.jbiosc.2016.07.009
Krug AW, Völker K, Dantzler WH, Silbernagl S (2007) Why is D-serine nephrotoxic and alpha-aminoisobutyric acid protective? Am J Physiol Renal Physiol 293:F382–F390. https://doi.org/10.1152/ajprenal.00441.2006
Lata S, Batra B, Pundir CS (2012) Construction of D-amino acid biosensor based on D-amino acid oxidase immobilized onto poly (indole-5-carboxylic acid)/zinc sulfide nanoparticles hybrid film. Process Biochem 47:2131–2138. https://doi.org/10.1016/j.ab.2013.01.030
Lee RJ, Hariri BM, McMahon DB, Chen B, Doghramji L, Adappa ND, Palmer JN, Kennedy DW, Jiang P, Margolskee RF, Cohen NA (2017) Bacterial D-amino acids suppress sinonasal innate immunity through sweet taste receptors in solitary chemosensory cells. Sci Signal 10:eaam7703. https://doi.org/10.1126/scisignal.aam7703
Levine S, Saltzman A (2003) Acute uremia produced in rats by nephrotoxic chemicals is alleviated by protein deficient diet. Ren Fail 25:517–523. https://doi.org/10.1081/jdi-120022542
Li G, Cui Y, You J, Zhao X, Sun Z, Xia L, Suo Y, Wang X (2011) Determination of trace amino acids in human serum by a selective and sensitive pre-column derivatization method using HPLC-FLD-MS/MS and derivatization optimization by response surface methodology. Amino Acids 40:1185–1193. https://doi.org/10.1007/s00726-010-0742-9
Liardon R, Hurrel RF (1983) Amino acid racemization in heated and alkali-treated proteins. J Agric Food Chem 31:432–437. https://doi.org/10.1021/jf00116a062
Linden G, Lorient D (1999) In: G. Linden and D. Lorient, (ed). New ingredients in food processing: biochemistry and agriculture. CRC press, Boca Raton, pp 184–210
Lüpke M, Brückner H (1998) Gas chromatographic evaluation of amino acid epimerisation in the course of gelatin manufacturing and processing. Z Lebensm Unters Forsch 206:323–328. https://doi.org/10.1007/s0021700502
MacKay MB, Paylor JW, Wong JTF, Winship IR, Baker GB, Dursun SM (2019) Multidimensional connectomics and treatment-resistant schizophrenia: linking phenotypic circuits to targeted therapeutics. Front Psychiatry 9:537–556. https://doi.org/10.3389/fpsyt.2018.00537
Marchelli R, Palla G, Dossena A, Galaverna G, Corradini R, Clementi S (1997) D-amino acids: molecular markers of ageing and authenticity for Parmigiano Reggiano and Grana Padano cheese. Sci Tecn Latt-Cas 48:21–32
Marchelli R, Galaverna G, Dossena A, Palla G, Bobbio A, Santaguida S, Grozeva K, Corradini R, Sforza S (2007) In: Konno R et al (eds) In: D-amino acids: a new frontier in amino acid and protein research. Nova Science Publishers, New York, pp 299–315
Marcone GL, Marinelli F (2014) Glycopeptides: an old but up to date successful antibiotic class. In: Marinelli F, Genilloud O (eds) Antimicrobials. Springer-Verlag, Berlin, pp 85–107
Martínez-Girón AB, García-Ruiz C, Crego AL, Marina ML (2009) Development of an in-capillary derivatization method by CE for the determination of chiral amino acids in dietary supplements and wines. Electrophoresis 30:696–704. https://doi.org/10.1002/elps.200800481
Masters PM, Friedman M (1979) Racemization of amino acids in alkali-treated food proteins. J Agric Food Chem 27:507–511
Miyoshi Y, Nagano M, Ishigo S, Ito Y, Hashiguchi K, Hishida N, Mita M, Lindner W, Hamase K (2014) Chiral amino acid analysis of Japanese traditional Kurozu and the developmental changes during earthenware jar fermentation processes. J Chromatogr B Anal Technol Biomed Life Sci 966:187–192. https://doi.org/10.1016/j.jchromb.2014.01.034
Mochizuki T, Todoroki K, Inoue K, Min JZ, Toyo'oka T (2014) Isotopic variants of light and heavy L-pyroglutamic acid succinimidyl esters as the derivatization reagents for DL-amino acid chiral metabolomics identification by liquid chromatography and electrospray ionization mass spectrometry. Anal Chim Acta 811:51–59. https://doi.org/10.1016/j.aca.2013.12.016
Mutaguchi Y, Ohmori T, Akano H, Doi K, Ohshima T (2013) Distribution of D-amino acids in vinegars and involvement of lactic acid bacteria in the production of D-amino acids. Springerplus 2:691–699. https://doi.org/10.1186/2193-1801-2-691
Mutaguchi Y, Kobayashi J, Oikawa T, Ohshima T (2016) D-amino acids in fermentative foods. In: Yoshimura T et al (eds) D-amino acids. Springer Tokyo, pp 341–357
Nakano Y, Konya Y, Taniguchi M, Fukusaki E (2017) Development of a liquid chromatography-tandem mass spectrometry method for quantitative analysis of trace D-amino acids. J Biosci Bioeng 123:134–138. https://doi.org/10.1016/j.jbiosc.2016.07.008
Ogawa T, Fukuda M (1973) Occurrence of D-amino acid aminotransferase in pea seedlings. Biochem Biophys Res Commun 52:998–1002. https://doi.org/10.1016/0006-291x(73)91036-x
Okada K, Gogami Y, Oikawa T (2013) Principal component analysis of the relationship between the D-amino acid concentrations and the taste of the sake. Amino Acids 44:489–498. https://doi.org/10.1007/s00726-012-1359-y
Opstvedt J, Miller R, Hardy RW, Spinelli J (1984) Heat-induced changes in sulfhydryl groups and disulfide bonds in fish protein and their effect on protein and amino acid digestibility in rainbow trout (Salmo gairdneri). J Agric Food Chem 32:929–935. https://doi.org/10.1021/jf00124a056
Palla G, Marchelli R, Dossena A, Casnati G (1989) Occurrence of D-amino acids in food: detection by capillary gas chromatography and by reversed-phase high-performance liquid chromatography with L-phenylalaninamides as chiral selectors. J Chrom A 475:45–53. https://doi.org/10.1016/S0021-9673(00)91414-6
Pätzold R, Brückner H (2006) Gas chromatographic determination and mechanism of formation of D-amino acids occurring in fermented and roasted cocoa beans, cocoa powder, chocolate and cocoa shell. Amino Acids 31:63–72. https://doi.org/10.1007/s00726-006-0330-1
Pawloska M, Armstrong DW (1994) Evaluation of enantiomeric purity of selected amino acids in honey. Chirality. 6:270–276. https://doi.org/10.1002/chir.530060409
Pidgeon SE, Fura JM, Leon W, Birabaharan M, Vezenov D, Pires MM (2015) Metabolic profiling of bacteria by unnatural C-terminated D-amino acids. Angew Chem Int Ed Eng 54:6158–6162. https://doi.org/10.1002/anie.201409927
Pollegioni L, Sacchi S (2010) Metabolism of the neuromodulator D-serine. Cell Mol Life Sci 67:2387–2404. https://doi.org/10.1007/s00018-010-0307-9
Pollegioni L, Piubelli L, Sacchi S, Pilone MS, Molla G (2007) Physiological functions of D-amino acid oxidases: from yeast to humans. Cell Mol Life Sci 64:1373–1394. https://doi.org/10.1007/s00018-007-6558-4
Prandi B, Faccini A, Lambertini F, Bencivenni M, Jorba M, Van Droogenbroek B, Bruggeman G, Schöber J, Petrusan J, Elst K, Sforza S (2019) Food wastes from agrifood industry as possible sources of proteins: a detailed molecular view on the composition of the nitrogen fraction, amino acid profile and racemisation degree of 39 food waste streams. Food Chem 286:567–575. https://doi.org/10.1016/j.foodchem.2019.01.166
Pundir CS, Lata S, Narwal V (2018) Biosensors for determination of D and L- amino acids: a review. Biosens Bioelectron 117:373–384. https://doi.org/10.1016/j.bios.2018.06.033
Rekoslavskaya NI, Yurjeva OV, Salyaev RK, Mapelli S, Kopytina TV (1999) D-tryptophan as IAA source during wheat germination. Bulg J Plant Physiol 25:39–49
Reynolds PE, Courvalin P (2005) Vancomycin resistance in enterococci due to synthesis of precursors terminating in D-alanyl-D-serine. Antimicrob Agents Chemother 49:20–25. https://doi.org/10.1128/AAC.49.1.21
Rosini E, Molla G, Rossetti C, Pilone MS, Pollegioni L, Sacchi S (2008) A biosensor for all D-amino acids using evolved D-amino acid oxidase. J Biotechnol 135:377–384. https://doi.org/10.1016/j.jbiotec.2008.06.001
Rozan P, Kuo YH, Lambein F (2000) Free amino acids present in commercially available seedlings sold for human consumption. A potential hazard for consumers. J Agric Food Chem 48:716–723. https://doi.org/10.1021/jf990729v
Rubio-Barroso S, Santosjj-Delgado MJ, Martín-Olivar C, Polo-Díez LM (2006) Indirect chiral HPLC determination and fluorimetric detection of D-amino acids in milk and oyster samples. J Dairy Sci 89:82–89. https://doi.org/10.3168/jds.S0022-0302(06)72071-9
Sacchi S, Pollegioni L, Pilone MS, Rossetti C (1998) Determination of D-amino acids using a D-amino acid oxidase biosensor with spectrophotometric and potentiometric detection. Biotechnol Tech 12:149–153
Sacchi S, Rosini E, Caldinelli L, Pollegioni L (2012) Biosensors for D-amino acid detection. Methods Mol Biol 794:313–324. https://doi.org/10.1007/978-1-61779-331-8_21
Sarkar P, Tothill IE, Setford SJ, Turner AP (1999) Screen-printed amperometric biosensors for the rapid measurement of L- and D-amino acids. Analyst. 124:865–870. https://doi.org/10.1039/A901404G
Sasamura T, Matsuda A, Kokuba Y (1998) Tumor growth inhibition and nutritional effect of D-amino acid solution in AH109A hepatoma-bearing rats. J Nutr Sci Vitaminol (Tokyo) 44:79–87. https://doi.org/10.1271/bbb.62.2418
Schiffman SS, Sennewald K, Gagnon J (1981) Comparison of taste qualities and thresholds of D- and L-amino acids. Physiol Behav 27:51–59. https://doi.org/10.1016/0031-9384(81)90298-5
Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477
Seo WH, Lee HG, Baek HH (2008) Evaluation of bitterness in enzymatic hydrolysates of soy protein isolate by taste dilution analysis. J Food Sci 73:41–43. https://doi.org/10.1111/j.1750-3841.2007.00610.x
Simó C, Martín-Alvarez PJ, Barbas C, Cifuentes A (2004) Application of stepwise discriminant analysis to classify commercial orange juices using chiral micellar electrokinetic chromatography-laser induced fluorescence data of amino acids. Electrophoresis 25:2885–2891
Solms J, Vuataz L, Egli RH (1965) The taste of L- and D-amino acids. Experentia XXI/12: 692-693
Taniguchi M, Konya Y, Nakano Y, Fukusaki E (2017) Investigation of storage time-dependent alterations of enenatioselective amino acid profiles in kimchi using liquid chromatography-time of flight mass spectrometry. J Biosci Bioeng 124:414–418. https://doi.org/10.1016/j.jbiosc.2017.04.019
Thippeswamy R, Gouda KG, Rao DH, Martin A, Gowda LR (2006) Determination of theanine in commercial tea by liquid chromatography with fluorescence and diode array ultraviolet detection. J Agric Food Chem 54:7014–7019
Tian H, Zheng N, Li S, Zhang Y, Zhao S, Wen F, Wang J (2017) Characterization of chiral amino acids from different milk origins using ultra-performance liquid chromatography coupled to ion-mobility mass spectrometry. Sci Rep 7:46289–46297. https://doi.org/10.1038/srep46289
Váradi M, Adányi N, Szabó EE, Trummer N (1999) Determination of the ratio of D- and L-amino acids in brewing by an immobilised amino acid oxidase enzyme reactor coupled to amperometric detection. Biosens Bioelectron 14:335–340. https://doi.org/10.1016/S0956-5663(98)00130-4
Visser WF, Verhoeven-Duif NM, Ophoff R, Bakker S, Klomp LW, Berger R, de Koning TJ (2011) A sensitive and simple ultra-high-performance-liquid chromatography-tandem mass spectrometry based method for the quantification of D-amino acids in body fluids. J Chromatogr A 1218:7130–7136. https://doi.org/10.1016/j.chroma.2011.07.087
Voss K, Galensa R (2000) Determination of L- and D-amino acids in foodstuffs by coupling of high-performance liquid chromatography with enzyme reactors. Amino Acids 18:339–352
Waldhier MC, Dettmer K, Gruber MA, Oefner PJ (2010) Comparison of derivatization and chromatographic methods for GC-MS analysis of amino acid enantiomers in physiological samples. J Chromatogr B Analyt Technol Biomed Life Sci. 878:1103–1112. https://doi.org/10.1016/j.jchromb.2010.03.021
Weisło M, Compagnone D, Trojanowicz M (2007) Enantioselective screen-printed amperometric biosensor for the determination of D-amino acids. Bioelectrochemistry. 71:91–98. https://doi.org/10.1016/j.bioelechem.2006.09.001
Williams RE, Lock EA (2004) D-serine-induced nephrotoxicity: possible interaction with tyrosine metabolism. Toxicology 201:231–238. https://doi.org/10.1016/j.tox.2004.05.001
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This work was supported by Fondazione Cariplo (Grant 2018-2786).
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Marcone, G.L., Rosini, E., Crespi, E. et al. D-amino acids in foods. Appl Microbiol Biotechnol 104, 555–574 (2020). https://doi.org/10.1007/s00253-019-10264-9
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DOI: https://doi.org/10.1007/s00253-019-10264-9