Skip to main content
SpringerLink
Log in

Fermentation of Gluten by Lactococcus lactis LLGKC18 Reduces its Antigenicity and Allergenicity

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Wheat is a worldwide staple food, yet some people suffer from strong immunological reactions after ingesting wheat-based products. Lactic acid bacteria (LAB) constitute a promising approach to reduce wheat allergenicity because of their proteolytic system. In this study, 172 LAB strains were screened for their proteolytic activity on gluten proteins and α-amylase inhibitors (ATIs) by SDS-PAGE and RP-HPLC. Gliadins, glutenins, and ATI antigenicity and allergenicity were assessed by Western blot/Dot blot and by degranulation assay using RBL-SX38 cells. The screening resulted in selecting 9 high gluten proteolytic strains belonging to two species: Enterococcus faecalis and Lactococcus lactis. Proteomic analysis showed that one of selected strains, Lc. lactis LLGKC18, caused degradation of the main gluten allergenic proteins. A significant decrease of the gliadins, glutenins, and ATI antigenicity was observed after fermentation of gluten by Lc. lactis LLGKC18, regardless the antibody used in the tests. Also, the allergenicity as measured by the RBL-SX38 cell degranulation test was significantly reduced. These results indicate that Lc. lactis LLGKC18 gluten fermentation can be deeply explored for its capability to hydrolyze the epitopes responsible for wheat allergy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this published article and comply with research standards.

References

  1. Longo G, Berti I, Burks AW et al (2013) IgE-mediated food allergy in children. Lancet 382:1656–1664. https://doi.org/10.1016/S0140-6736(13)60309-8

    Article  CAS  PubMed  Google Scholar 

  2. Czaja-Bulsa G, Bulsa M (2017) What do we know now about IgE-mediated wheat allergy in children? Nutrients 9:1–9. https://doi.org/10.3390/nu9010035

    Article  CAS  Google Scholar 

  3. Osborne TB (1924) The Vegetable proteins. Longmans Green and Co, London

    Google Scholar 

  4. Tatham AS, Shewry PR (2008) Allergens to wheat and related cereals. Clin Exp Allergy 38:1712–1726. https://doi.org/10.1111/j.1365-2222.2008.03101.x

    Article  CAS  PubMed  Google Scholar 

  5. Cianferoni A (2016) Wheat allergy: Diagnosis and management. J Asthma Allergy 9:13–25. https://doi.org/10.2147/JAA.S81550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lupi R, Denery-Papini S, Claude M et al (2019) Thermal treatment reduces gliadin recognition by IgE but a subsequent digestion and epithelial crossing permits recovery. Food Res Int 118:22–31. https://doi.org/10.1016/j.foodres.2018.02.011

    Article  CAS  PubMed  Google Scholar 

  7. Marco ML, Sanders ME, Gänzle M et al (2021) The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on fermented foods. Nat Rev Gastroenterol Hepatol 196:208–218. https://doi.org/10.1038/s41575-020-00390-5

    Article  Google Scholar 

  8. Ogunsakin AO, Vanajakshi V, Anu-Appaiah KA et al (2017) Evaluation of functionally important lactic acid bacteria and yeasts from Nigerian sorghum as starter cultures for gluten-free sourdough preparation. LWT Food Sci Technol 82:326–334. https://doi.org/10.1016/j.lwt.2017.04.048

    Article  CAS  Google Scholar 

  9. Gerez CL, Rollán GC, De Valdez GF (2006) Gluten breakdown by lactobacilli and pediococci strains isolated from sourdough. Lett Appl Microbiol 42:459–464. https://doi.org/10.1111/j.1472-765X.2006.01889.x

    Article  CAS  PubMed  Google Scholar 

  10. Rollán G, De Angelis M, Gobbetti M, De Valdez GF (2005) Proteolytic activity and reduction of gliadin-like fractions by sourdough lactobacilli. J Appl Microbiol 99:1495–1502. https://doi.org/10.1111/j.1365-2672.2005.02730.x

    Article  CAS  PubMed  Google Scholar 

  11. Poutanen K, Flander L, Katina K (2009) Sourdough and cereal fermentation in a nutritional perspective. Food Microbiol 26:693–699. https://doi.org/10.1016/j.fm.2009.07.011

    Article  CAS  PubMed  Google Scholar 

  12. Rizzello CG, De Angelis M, Di Cagno R et al (2007) Highly efficient gluten degradation by lactobacilli and fungal proteases during food processing: new perspectives for celiac disease. Appl Environ Microbiol 73:4499–4507. https://doi.org/10.1128/AEM.00260-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zotta T, Piraino P, Ricciardi A et al (2006) Proteolysis in model sourdough fermentations. J Agric Food Chem 54:2567–2574. https://doi.org/10.1021/jf052504s

    Article  CAS  PubMed  Google Scholar 

  14. Greco L, Gobbetti M, Auricchio R et al (2011) Safety for patients with celiac disease of baked goods made of wheat flour hydrolyzed during food processing. Clin Gastroenterol Hepatol 9:24–29. https://doi.org/10.1016/j.cgh.2010.09.025

    Article  PubMed  Google Scholar 

  15. Stefańska I, Piasecka-Jóźwiak K, Kotyrba D et al (2016) Selection of lactic acid bacteria strains for the hydrolysis of allergenic proteins of wheat flour. J Sci Food Agric 96:3897–3905. https://doi.org/10.1002/jsfa.7588

    Article  CAS  PubMed  Google Scholar 

  16. De Angelis M, Rizzello CG, Scala E et al (2007) Probiotic preparation has the capacity to hydrolyze proteins responsible for wheat allergy. J Food Prot 70:135–144. https://doi.org/10.4315/0362-028X-70.1.135

    Article  PubMed  Google Scholar 

  17. Nagano H, Kasuya S, Shoji Z et al (2003) Identification of microorganisms in traditional Asian foods made with fermented wheat flour and their hypoallergenization. Food Sci Technol Res 9:7–10. https://doi.org/10.3136/fstr.9.7

    Article  Google Scholar 

  18. Fira D, Kojic M, Banina A et al (2001) Characterization of cell envelope-associated proteinases of thermophilic lactobacilli. J Appl Microbiol 90:123–130. https://doi.org/10.1046/j.1365-2672.2001.01226.x

    Article  CAS  PubMed  Google Scholar 

  19. El-Ghaish S, Dalgalarrondo M, Choiset Y et al (2010) Screening of strains of lactococci isolated from Egyptian dairy products for their proteolytic activity. Food Chem 120:758–764. https://doi.org/10.1016/j.foodchem.2009.11.007

    Article  CAS  Google Scholar 

  20. Todorov SD, Wachsman M, Tomé E et al (2010) Characterisation of an antiviral pediocin-like bacteriocin produced by Enterococcus faecium. Food Microbiol 27:869–879. https://doi.org/10.1016/j.fm.2010.05.001

    Article  CAS  PubMed  Google Scholar 

  21. Langella O, Valot B, Balliau T et al (2017) X!TandemPipeline: a tool to manage sequence redundancy for protein inference and phosphosite identification. J Proteome Res 16:494–503. https://doi.org/10.1021/acs.jproteome.6b00632

    Article  CAS  PubMed  Google Scholar 

  22. Tranquet O, Larré C, Denery-Papini S (2012) Selection of a monoclonal antibody for detection of gliadins and glutenins: a step towards reliable gluten quantification. J Cereal Sci 56:760–763. https://doi.org/10.1016/j.jcs.2012.07.005

    Article  CAS  Google Scholar 

  23. Larre C, Lupi R, Denery S, Tranquet O, Masci S, (2019) Production of antibodies against functional recombinant wheat ATIs. In: Koehler P (Ed) Working group on prolamin analysis and toxicity (WGPAT). Peter Kohler, Urbino, p 53–60

  24. Wiegand TW, Williams PB, Dreskin SC et al (1996) High-affinity oligonucleotide ligands to human IgE inhibit binding to Fc epsilon receptor I. J Immunol 157:221–230 (PMID: 8683119)

    CAS  PubMed  Google Scholar 

  25. Tranquet O (2020) Anticorps chimériques dirigés contre des séquences des domaines répétés des gliadines pour mimer la réactivité des IgE de patients allergiques au blé. Université de Nantes, France

    Google Scholar 

  26. Binaghi RA, Demeulemester C (1983) Influence of the medium on the heat and acid denaturation of IgE. J Immunol Methods 65:225–233. https://doi.org/10.1016/0022-1759(83)90319-8

    Article  CAS  PubMed  Google Scholar 

  27. Lupi R, Denery-Papini S, Claude M et al (2019) Thermal treatment reduces gliadin recognition by IgE, but a subsequent digestion and epithelial crossing permits recovery. Food Res Int 118:22–31. https://doi.org/10.1016/j.foodres.2018.02.011

    Article  CAS  PubMed  Google Scholar 

  28. Bodinier M, Brossard C, Triballeau S et al (2008) Evaluation of an in vitro mast cell degranulation test in the context of food allergy to wheat. Int Arch Allergy Immunol 146:307–320. https://doi.org/10.1159/000121465

    Article  CAS  PubMed  Google Scholar 

  29. Brouns F, van Rooy G, Shewry P et al (2019) Adverse reactions to wheat or wheat components. Compr Rev Food Sci Food Saf 18:1437–1452. https://doi.org/10.1111/1541-4337.12475

    Article  PubMed  Google Scholar 

  30. Tanabe S (2004) IgE-binding abilities of pentapeptides, QQPFP and PQQPF, in wheat gliadin. J Nutr Sci Vitaminol (Tokyo) 50:367–370. https://doi.org/10.3177/jnsv.50.367

    Article  CAS  Google Scholar 

  31. Matsuo H, Yokooji T, Taogoshi T (2015) Common food allergens and their IgE-binding epitopes. Allergol Int 64:332–343. https://doi.org/10.1016/j.alit.2015.06.009

    Article  CAS  PubMed  Google Scholar 

  32. Denery-Papini S, Bodinier M, Pineau F et al (2011) Immunoglobulin-E-binding epitopes of wheat allergens in patients with food allergy to wheat and in mice experimentally sensitized to wheat proteins. Clin Exp Allergy 41:1478–1492. https://doi.org/10.1111/j.1365-2222.2011.03808.x

    Article  CAS  PubMed  Google Scholar 

  33. Battais F, Pineau F, Popineau Y et al (2003) Food allergy to wheat: Identification of immunogloglin E and immunoglobulin G-binding proteins with sequential extracts and purified proteins from wheat flour. Clin Exp Allergy 33:962–970. https://doi.org/10.1046/j.1365-2222.2003.01592.x

    Article  CAS  PubMed  Google Scholar 

  34. Dupont FM, Vensel WH, Tanaka CK et al (2011) Deciphering the complexities of the wheat flour proteome using quantitative two-dimensional electrophoresis, three proteases and tandem mass spectrometry. Proteome Sci 9:1–29. https://doi.org/10.1186/1477-5956-9-10

    Article  CAS  Google Scholar 

  35. Schalk K, Lexhaller B, Koehler P, Scherf KA (2017) Isolation and characterization of gluten protein types from wheat, rye, barley and oats for use as reference materials. PLoS ONE 12:1–20. https://doi.org/10.1371/journal.pone.0172819

    Article  CAS  Google Scholar 

  36. Tundo S, Lupi R, Lafond M et al (2018) Wheat ati CM3, CM16 and 0.28 allergens produced in Pichia pastoris display a different eliciting potential in food allergy to wheat. Plants 7:1–13. https://doi.org/10.3390/plants7040101

    Article  CAS  Google Scholar 

  37. Weegels PL, Hamer RJ, Schofield JD (1997) Depolymerisation and re-polymerisation of wheat glutenin during dough processing. II. Changes in composition J Cereal Sci 25:155–163. https://doi.org/10.1006/jcrs.1996.0082

    Article  CAS  Google Scholar 

  38. El-Ghaish S, Rabesona H, Choiset Y et al (2011) Proteolysis by Lactobacillus fermentum IFO3956 isolated from Egyptian milk products decreases immuno-reactivity of αS1-casein. J Dairy Res 78:203–210. https://doi.org/10.1017/S0022029911000100

    Article  CAS  PubMed  Google Scholar 

  39. Liu J, Zhou J, Wang L et al (2017) Improving nitrogen source utilization from defatted soybean meal for nisin production by enhancing proteolytic function of Lactococcus lactis F44. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-06537-w

    Article  CAS  Google Scholar 

  40. Huang X, Schuppan D, Tovar LER et al (2020) Sourdough fermentation degrades wheat alpha-amylase/trypsin inhibitor (ATI) and reduces pro-inflammatory activity. Foods 9:943. https://doi.org/10.3390/foods9070943

    Article  CAS  PubMed Central  Google Scholar 

  41. Herrán AR, Pérez-Andrés J, Caminero A et al (2017) Gluten-degrading bacteria are present in the human small intestine of healthy volunteers and celiac patients. Res Microbiol 168:673–684. https://doi.org/10.1016/j.resmic.2017.04.008

    Article  CAS  PubMed  Google Scholar 

  42. Wieser H (2007) Chemistry of gluten proteins. Food Microbiol 24:115–119. https://doi.org/10.1016/j.fm.2006.07.004

    Article  CAS  PubMed  Google Scholar 

  43. Mika N, Zorn H, Rühl M (2015) Prolyl-specific peptidases for applications in food protein hydrolysis. Appl Microbiol Biotechnol 99:7837–7846. https://doi.org/10.1007/s00253-015-6838-0

    Article  CAS  PubMed  Google Scholar 

  44. Guillot A, Boulay M, Chambellon É et al (2016) Mass Spectrometry analysis of the extracellular peptidome of Lactococcus lactis: lines of evidence for the coexistence of extracellular protein hydrolysis and intracellular peptide excretion. J Proteome Res 15:3214–3224. https://doi.org/10.1021/acs.jproteome.6b00424

    Article  CAS  PubMed  Google Scholar 

  45. Liu M, Bayjanov JR, Renckens B et al (2010) The proteolytic system of lactic acid bacteria revisited: A genomic comparison. BMC Genomics 11:5–8. https://doi.org/10.1186/1471-2164-11-36

    Article  CAS  Google Scholar 

  46. Meijer W, Marugg JD, Hugenholtz J (1996) Regulation of proteolytic enzyme activity in Lactococcus lactis. Appl Environ Microbiol 62:156–161. https://doi.org/10.1128/aem.62.1.156-161.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kiefer-Partsch B, Bockelmann W, Geis A, Teuber M (1989) Purification of an X-prolyl-dipeptidyl aminopeptidase from the cell wall proteolytic system of Lactococcus lactis subsp cremoris. Appl Microbiol Biotechnol 31:75–78. https://doi.org/10.1007/BF00252531

    Article  CAS  Google Scholar 

  48. Phromraksa P, Nagano H, Boonmars T, Kamboonruang C (2008) Identification of proteolytic bacteria from thai traditional fermented foods and their allergenic reducing potentials. J Food Sci 73(4):M189–M195. https://doi.org/10.1111/j.1750-3841.2008.00721.x

    Article  CAS  PubMed  Google Scholar 

  49. Fu W, Rao H, Tian Y, Xue W (2020) Bacterial composition in sourdoughs from different regions in China and the microbial potential to reduce wheat allergens. LWT Food Sci Technol 117:108669. https://doi.org/10.1016/j.lwt.2019.108669

    Article  CAS  Google Scholar 

  50. P Carbonero F García-Olmedo 1999 A multigene family of trypsin/α-amylase inhibitors from cereals Seed Proteins 617–633 https://doi.org/10.1007/978-94-011-4431-5_26

  51. Breiteneder H, Radauer C (2004) A classification of plant food allergens. J Allergy Clin Immunol 113:821–830. https://doi.org/10.1016/j.jaci.2004.01.779

    Article  CAS  PubMed  Google Scholar 

  52. Cuccioloni M, Mozzicafreddo M, Ali I et al (2016) Interaction between wheat alpha-amylase/trypsin bi-functional inhibitor and mammalian digestive enzymes: kinetic equilibrium and structural characterization of binding. Food Chem 213:571–578. https://doi.org/10.1016/j.foodchem.2016.07.020

    Article  CAS  PubMed  Google Scholar 

  53. Caminero A, McCarville JL, Zevallos VF et al (2019) Lactobacilli degrade wheat amylase trypsin inhibitors to reduce intestinal dysfunction induced by immunogenic wheat proteins. Gastroenterology 156:2266–2280. https://doi.org/10.1053/j.gastro.2019.02.028

    Article  CAS  PubMed  Google Scholar 

  54. Valenta R, Hochwallner H, Linhart B, Pahr S (2015) Food allergies: the basics. Gastroenterology 148:1120-1131.e4. https://doi.org/10.1053/j.gastro.2015.02.006

    Article  CAS  PubMed  Google Scholar 

  55. Kazemi R, Taheri-Kafrani A, Motahari A, Kordesedehi R (2018) Allergenicity reduction of bovine milk β-lactoglobulin by proteolytic activity of lactococcus lactis BMC12C and BMC19H isolated from Iranian dairy products. Int J Biol Macromol 112:876–881. https://doi.org/10.1016/j.ijbiomac.2018.02.044

    Article  CAS  PubMed  Google Scholar 

  56. Tulini FL, Bíscola V, Choiset Y et al (2015) Evaluation of the proteolytic activity of Enterococcus faecalis FT132 and Lactobacillus paracasei FT700 isolated from dairy products in Brazil using milk proteins as substrates. Eur Food Res Technol 241:385–392. https://doi.org/10.1007/s00217-015-2470-6

    Article  CAS  Google Scholar 

  57. Biscola V, de Olmos AR, Choiset Y et al (2017) Soymilk fermentation by Enterococcus faecalis VB43 leads to reduction in the immunoreactivity of allergenic proteins β-conglycinin (7S) and glycinin (11S). Benef Microbes 8:635–643. https://doi.org/10.3920/BM2016.0171

    Article  CAS  PubMed  Google Scholar 

  58. Rizzello CG, De Angelis M, Coda R, Gobbetti M (2006) Use of selected sourdough lactic acid bacteria to hydrolyze wheat and rye proteins responsible for cereal allergy. Eur Food Res Technol 223:405–411. https://doi.org/10.1007/s00217-005-0220-x

    Article  CAS  Google Scholar 

  59. V Bradauskiene L Vaiciulyte-Funk E Mazoniene D Cernauskas 2019 Fermentation with lactobacillus strains for elimination of gluten in wheat (Triticum Aestivum) by-products Food Balt 109–114 https://doi.org/10.22616/foodbalt.2019.029

  60. Cabanillas B, Cuadrado C, Rodriguez J et al (2015) Potential changes in the allergenicity of three forms of peanut after thermal processing. Food Chem 183:18–25. https://doi.org/10.1016/j.foodchem.2015.03.023

    Article  CAS  PubMed  Google Scholar 

  61. Matsuo H, Morita E, Tatham AS et al (2004) Identification of the IgE-binding epitope in ω-5 Gliadin, a major allergen in wheat-dependent exercise-induced anaphylaxis. J Biol Chem 279:12135–12140. https://doi.org/10.1074/jbc.M311340200

    Article  CAS  PubMed  Google Scholar 

  62. Altenbach SB, Chang HC, Simon-Buss A et al (2018) Towards reducing the immunogenic potential of wheat flour: omega gliadins encoded by the D genome of hexaploid wheat may also harbor epitopes for the serious food allergy WDEIA. BMC Plant Biol 18:1–12. https://doi.org/10.1186/s12870-018-1506-z

    Article  CAS  Google Scholar 

  63. Cho K, Beom HR, Jang YR et al (2018) Proteomic profiling and epitope analysis of the complex α- γ- and ω-gliadin families in a commercial bread wheat. Front Plant Sci 9:1–15. https://doi.org/10.3389/fpls.2018.00818

    Article  Google Scholar 

  64. Fu W, Rao H, Tian Y, Xue W (2020) Bacterial composition in sourdoughs from different regions in China and the microbial potential to reduce wheat allergens. LWT-Food Sci Technol 117:108669. https://doi.org/10.1016/j.lwt.2019.108669

    Article  CAS  Google Scholar 

  65. De Angelis M, Cassone A, Rizzello CG et al (2010) Mechanism of degradation of immunogenic gluten epitopes from Triticum turgidum L. var. durum by sourdough lactobacilli and fungal proteases. Appl Environ Microbiol 76:508–518. https://doi.org/10.1128/AEM.01630-09

    Article  CAS  PubMed  Google Scholar 

  66. Sakandar HA, Usman K, Imran M (2018) Isolation and characterization of gluten-degrading Enterococcus mundtii and Wickerhamomyces anomalus, potential probiotic strains from indigenously fermented sourdough (Khamir). LWT - Food Sci Technol 91:271–277. https://doi.org/10.1016/j.lwt.2018.01.023

    Article  CAS  Google Scholar 

  67. Schuppan D, Pickert G, Ashfaq-Khan M, Zevallos V (2015) Non-celiac wheat sensitivity: Differential diagnosis, triggers and implications. Best Pract Res Clin Gastroenterol 29:469–476. https://doi.org/10.1016/j.bpg.2015.04.002

    Article  CAS  PubMed  Google Scholar 

  68. Junker Y, Zeissig S, Kim SJ et al (2012) Wheat amylase trypsin inhibitors drive intestinal inflammation via activation of toll-like receptor 4. J Exp Med 209:2395–2408. https://doi.org/10.1084/jem.20102660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors wish to acknowledge Gilbert Deshayes for his technical help to perform the RP-HPLC analysis. Emilie Perrin for her help in IgE quantification and Marion Deffrasnes for her technical help in the microbiology tests.

Funding

This research was funded by RFI Food For Tomorrow: FerAll project and FAPESP (Sao Paulo Research Foundation, projects 2018/11475–3).

Author information

Authors and Affiliations

  1. INRAE UR1268 BIA, Rue de la Géraudière, BP 71627, 44316, Nantes, France

    Kamel-Eddine El Mecherfi, Roberta Lupi, Mehdi Cherkaoui, Olivier Tranquet, Hélène Rogniaux, Sandra Denery-Papini & Colette Larré

  2. Applied Molecular Genetics Department, USTO Mohamed BOUDIAF University, Oran, Algeria

    Kamel-Eddine El Mecherfi

  3. Food Research Center, Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of Sao Paulo, Sao Paulo, SP, Brazil

    Marcela A. C. Albuquerque, Svetoslav Dimitrov Todorov & Bernadette Dora Gombossy de Melo Franco

  4. ProBacLab, Handong Global University, Pohang, Republic of Korea

    Svetoslav Dimitrov Todorov

  5. Synlab Provence, 13006, Marseille, France

    Caroline Klingebiel

  6. Food Microbiology Laboratory ONIRIS, Nantes, France

    Bernard Onno

Authors
  1. Kamel-Eddine El Mecherfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberta Lupi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mehdi Cherkaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcela A. C. Albuquerque
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Svetoslav Dimitrov Todorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Olivier Tranquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Caroline Klingebiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hélène Rogniaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sandra Denery-Papini
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bernard Onno
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Bernadette Dora Gombossy de Melo Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Colette Larré
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: K.E. and C.L.; methodology: K.E., R.L., M.C., H.R., M.C.A., S.T, C.L.; software handling: K.E., C.L.; writing—original draft preparation: K.E.; writing—review and editing: all authors; visualization, K.E.; supervision, K.E., C.L.; funding acquisition: C.L., K.E., B.O, and B.F. All authors have read and agreed to the last version of the manuscript.”

Corresponding author

Correspondence to Colette Larré.

Ethics declarations

Ethical Approval

This article does not contain any studies with human or animal subjects.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 217 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Mecherfi, KE., Lupi, R., Cherkaoui, M. et al. Fermentation of Gluten by Lactococcus lactis LLGKC18 Reduces its Antigenicity and Allergenicity. Probiotics & Antimicro. Prot. 14, 779–791 (2022). https://doi.org/10.1007/s12602-021-09808-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09808-1

Keywords

Search

Navigation