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Prophylactic properties of Bacillus subtilis in a bovine β-lactoglobulin sensitized mice model

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Abstract

Probiotics have gained considerable attention in recent years due to their biotechnological and immunomodulatory properties. The proteolytic activity and the protective effect of Bacillus subtilis isolated from Algerian goat milk preventing the development of allergic reactions were determined. On the base of SDS–PAGE analysis and the increase of detectable α-NH2 groups, it can be concluded that the isolated isolate has high proteolytic activity. Oral administration of studied Bacillus subtilis DAF442 resulted in significantly lower titers of anti β-lactoglobulin IgG and IgE. This was correlated with a significant decrease in the anaphylactic response ex vivo as measured by reduced short circuit current (Isc) and epithelial conductance (G) and in vivo in mice. Bacillus subtilis DAF442 pretreatment promoted an important protection against changes in intestinal morphology induced by β-lactoglobulin. Hence it can be concluded that studied Bacillus subtilis strain with high proteolytic activity can modulate effectively the immune response and prevent allergic reactions against β-lactoglobulin.

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References

  1. Platts-Mills TAE (2015) J Allergy Clin Immunol 136:3–13

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hochwallner H, Schulmeister U, Swoboda I, Spitzauer S, Valenta R (2014) Methods 66:22–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Virta LJ, Ashorn M, Kolho KL (2013) J Pediatr Gastroenterol Nutr 56:649–651

    Article  PubMed  Google Scholar 

  4. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2010) Gastroenterol 139:1844–1854

    Article  Google Scholar 

  5. Levy R, Borenstein E (2014) Gut Microbes 5:37–41

    Article  Google Scholar 

  6. Jackson M, Jeffery IB, Beaumont M, Bell JT, Clark AG, Ley RE, O’Toole PW, Spector TD, Steves CJ (2016) Genome Med 8:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ivakhnenko ES (2013) Nian’kovskiĭ SL. Georgian Med News 219:46–52

    Google Scholar 

  8. Martin CR, Ling PR, Blackburn GL (2016) Nutrients 8:279–289

    Article  CAS  PubMed Central  Google Scholar 

  9. Cutting SM (2011) Food Microbiol 28:214–220

    Article  PubMed  Google Scholar 

  10. Hong HA, Le Duc H, Cutting SM (2005) FEMS Microbiol Rev 29:813–835

    Article  CAS  PubMed  Google Scholar 

  11. Tompkins TA, Xu X, Ahmarani J (2010) Benef Microbes 1:93–106

    Article  CAS  PubMed  Google Scholar 

  12. Gu Y, Xu X, Wu Y, Niu T, Liu Y, Li J, Du G, Liu L (2018) Metab Eng https://doi.org/10.1016/j.ymben.2018.05.006

    Article  PubMed  Google Scholar 

  13. Hemberger S, Pedrolli DB, Stolz J, Vogl C, Lehmann M, Mack M (2011) BMC Biotechnol 11:119. https://doi.org/10.1186/1472-6750-11-119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhu F, Cai J, Wu X, Huang J, Huang L, Zhud J, Zheng Q, Cen P, Xu Z (2013) J Biotechnol 164:67–74

    Article  CAS  PubMed  Google Scholar 

  15. Xu Z, Feng X, Zhang D, Tang B, Lei P, Liang J, Xu H (2014) Bioresour Technol 155:8–14

    Article  CAS  PubMed  Google Scholar 

  16. Fu J, Wang Z, Chen T, Liu W, Shi T, Wang G, Tang Y, Zhao X (2014) Biotechnol Bioeng 111:2126–2131

    Article  CAS  PubMed  Google Scholar 

  17. Zhang X, Zhang R, Bao T, Rao Z, Yang T, Xu M, Xu Z, Li H, Yang S (2014) Metab Eng 23:34–41

    Article  CAS  PubMed  Google Scholar 

  18. Dib W, Chekroun A, El-Ghaish S, Choiset Y, Chobert J-M, Haertlé T, Saidi D, Kheroua O (2014) Int J Pharm Pharm Sci 6:587–590

    Google Scholar 

  19. El-Ghaish S, Dalgalarrondo M, Choiset Y, Sitohy M, Ivanova I, Haertlé T, Chobert J-M (2010) Eur Food Res Technol 230:635–643

    Article  CAS  Google Scholar 

  20. Laemmli UK (1970) Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  21. Doi E, Shibata D, Matoba T (1981) Anal Biochem 118:173–184

    Article  CAS  PubMed  Google Scholar 

  22. Zellal D, Kaddouri H, Grar H, Belarbi H, Kheroua O, Saidi D (2011) Food Agric Immunol 22:355–363

    Article  CAS  Google Scholar 

  23. Adel-Patient K, Créminon C, Bernard H, Clément G, Négroni L, Frobert Y, Grassi J, Wal JM, Chatel JM (2000) J Immunol Methods 235:21–32

    Article  CAS  PubMed  Google Scholar 

  24. Negaoui H, Kaddouri H, Kheroua O, Saidi D (2009) Am J Immunol 5:56–60

    Article  Google Scholar 

  25. Grar H, Dib W, El Mecherfi KE, Negaoui H, Gourine H, Bekkaddour Benattia S, Amier L, Kaddouri H, Kheroua O, Saidi D (2015) Eur Food Res Technol 241:393–398

    Article  CAS  Google Scholar 

  26. Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA (1999) J Allergy Clin Immunol 103:206–214

    Article  CAS  PubMed  Google Scholar 

  27. Priest F (1977) Bacteriol Rev 41:711–753

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Schallmey M, Singh A, Ward OP (2004) Can J Microbiol 50:1–17

    Article  CAS  PubMed  Google Scholar 

  29. Li W, Zhou X, Lu P (2004) Res Microbiol 155:605–610

    Article  CAS  PubMed  Google Scholar 

  30. Nijland R, Kuipers O (2008) Recent Pat Biotechnol 2:79–87

    Article  CAS  PubMed  Google Scholar 

  31. Chantawannakul P, Oncharoen A, Klanbut K, Chukeatirote E, Lumyong S (2002) Sci Asia 28:241–245

    Article  CAS  Google Scholar 

  32. Gaustevora A, Braikova D, Christov P, Tishinov K, Tonkova EV, Haertlé T, Nedkov P (2005) Lett Appl Microbiol 40:335–340

    Article  CAS  Google Scholar 

  33. Kamoun AS, Haddar A, Ali NEH, Basma FG, Kanoun S, Nasri M (2008) Microbiol Res 163:299–306

    Article  CAS  Google Scholar 

  34. Kramer JM, Gilbert RJ (1989) In: Doyle MP (ed) Foodborne bacterial pathogens. Marcel Dekker, New York

    Google Scholar 

  35. Denner WHB, Gillanders TGE (1996) In: Godfrey T, West S (eds) The Macmillan Press Ltd, 2nd edn. Basingstoke, UK

    Google Scholar 

  36. Zhou Z, Song Y, Mao C, Srivastava KD, Liu C, Yang N, Li XM (2015) Clin Immunol 135(2):AB29

    Google Scholar 

  37. Huang JM, La Ragione RM, Nunez A, Cutting SM (2008) FEMS Immunol Med Microbiol 53:195–203

    Article  CAS  PubMed  Google Scholar 

  38. Mehrad B, Standiford TJ (1999) Immunol Res 20:15–27

    Article  CAS  PubMed  Google Scholar 

  39. Sadler AJ, Williams BR (2008) Nat Rev Immunol 8:559–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Michail S (2009) Allergy Asthma Clin Immunol 5:5

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tang RB, Chen SJ (2001) Ann Allergy Asthma Immunol 86:314–317

    Article  CAS  PubMed  Google Scholar 

  42. Hu CH, Gu LY, Luan ZS, Song J, Zhu K (2012) Anim Feed Sci Technol 177:108–115

    Article  CAS  Google Scholar 

  43. Saïdi D, Heyman M, Kheroua O, Boudraa G, Bylsma P, Kerroucha R, Chekroun A, Maragi JA, Touhami M, Desjeux JF (1995) CR Acad Sci III 318:683–690

    Google Scholar 

  44. El Mecherfi KE, Rouaud O, Curet S, Negaoui H, Chobert J-M, Kheroua O, Saidi D, Haertlé T (2014) Int J Food Sci Technol 5:356–364

    Google Scholar 

  45. Crowe SE, Perdue MH (1992) Gastroenterol 103:1075–1095

    Article  CAS  Google Scholar 

  46. Schiffer C, Lalanne AI, Cassard L, Mancardi DA, Malbec O, Bruhns P, Dif F, Daeron M (2011) J Immunol 187:2646–2655

    Article  CAS  PubMed  Google Scholar 

  47. Forsythe P, Wang B, Khambati I, Kunze WA (2012) PLoS One 7:e41234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Oksaharju A, Kankainen M, Kekkonen RA, Lindstedt KA, Kovanen PT, Korpela R, Miettinen M (2011) World J Gastroenterol 17:750–759

    Article  PubMed  PubMed Central  Google Scholar 

  49. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, DeSimone C (2001) Gastroenterol 121:580–591

    Article  CAS  Google Scholar 

  50. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, Looijer-van Langen M, Kadsen KL (2008) Am J Physiol Gastrointest Liver Physiol 295:G1025–G1034

    Article  CAS  PubMed  Google Scholar 

  51. Sanchez B, Arias S, Chaignepain S, Denayrolles M, Schmitter JM, Bressollier P, Urdaci MC (2009) Microbiol 155:1708–1716

    Article  CAS  Google Scholar 

  52. Fujiya M, Musc MW, Nakagawa Y, Hu S, Alverdy J, Kohgo Y, Schneewind O, Jabri B, Chang EB (2007) Cell Host Microbe 1:299–308

    Article  CAS  PubMed  Google Scholar 

  53. Hosoi T, Hirose R, Saegusa S, Ametani A, Kiuchi K, Kaminogawa S (2003) Int J Food Microbiol 82:255–264

    Article  CAS  PubMed  Google Scholar 

  54. Urdaci MC, Bressollier P, Pinchuk I (2004) J Clin Gastroenterol 38:S86–S90

    Article  PubMed  Google Scholar 

  55. Fiorini G, Cimminiello C, Chianese R, Visconti GP, Cova D, Uberti T, Gibelli A (1985) Chemioterapia 4:310–312

    CAS  PubMed  Google Scholar 

  56. Le Duc H, Hong HA, Barbosa TM, Henriques AO, Cutting SM (2004) Appl Environ Microbiol 70:2161–2171

    Article  CAS  PubMed Central  Google Scholar 

  57. Hong HA, Khaneja R, Tam NM, Cazzato A, Tan S, Urdaci M, Brisson A, Gasbarrini A, Barnes I, Cutting SM (2009) Res Microbiol 160:134–143

    Article  CAS  PubMed  Google Scholar 

  58. Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A, Beyer K, Burks W, Canonica GW, Ebisawa M, Gandhi S, Kamenwa R, Lee BW, Li H, Prescott S, Riva JJ, Rosenwasser L, Sampson H, Spigler M, Terracciano L, Vereda-Ortiz A, Waserman S, Yepes-Nuñez JJ, Brożek JL, Schünemann HJ (2015) World Allergy Organ J 8:4

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was provided through the Franco-Algerian TASSILI cooperation project #10MDU 792 “Alimentation de l’enfant allergique: Allergénicité des protéines du lait bovin après traitements technologiques et étude du rôle prophylactique des laits hypoallergéniques chez le modèle animal d’allergie et les enfants à risque”. This work would not have been possible without the financial support of the Directorate General for Scientific Research and Technological Development (DGRSDT, MESRS, Algeria).

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Authors and Affiliations

  1. Laboratory of the Physiology of Nutrition and Food Safety, Department of Biology, Faculty of Natural and Life Science, University of Oran 1, Ahmed Ben Bella, Oran, Algeria

    Wafaa Dib, Hadria Grar, Hanane Gourine, Kamel Eddine El Mecherfi, Hanane Negaoui, Hanane Kaddouri, Djamel Saidi & Omar Kheroua

  2. Department of Biotechnology, Faculty of Natural and Life Science, University of Science and Technology Mohamed Boudiaf, Oran, Algeria

    Wafaa Dib

  3. Department of Biology, Faculty of Science, University of Mostaganem, BP 227, Mostaganem, Algeria

    Hadria Grar

  4. Department of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, SP, Brazil

    Vanessa Biscola

  5. UR 1268, Biopolymères Interactions Assemblages, INRA, 44300, Nantes, France

    Jean-Marc Chobert & Thomas Haertlé

  6. Department of Animal Nutrition and Feed Management, Poznan University of Life Sciences, ul. Wołyńska 33, 60-637, Poznań, Poland

    Thomas Haertlé

  7. Institute of Biochemistry and Biophysics, University of Teheran, Tehran, Iran

    Thomas Haertlé

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  1. Wafaa Dib
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Correspondence to Wafaa Dib.

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The experiments described in this study comply with the current Algerian legislation covering the protection of animals.

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Dib, W., Grar, H., Gourine, H. et al. Prophylactic properties of Bacillus subtilis in a bovine β-lactoglobulin sensitized mice model. Eur Food Res Technol 245, 1357–1364 (2019). https://doi.org/10.1007/s00217-019-03259-3

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  • DOI: https://doi.org/10.1007/s00217-019-03259-3

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