Advertisement

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

  • Wafaa DibEmail author
  • Hadria Grar
  • Hanane Gourine
  • Kamel Eddine El Mecherfi
  • Hanane Negaoui
  • Vanessa Biscola
  • Hanane Kaddouri
  • Jean-Marc Chobert
  • Thomas Haertlé
  • Djamel Saidi
  • Omar Kheroua
Original Paper
  • 54 Downloads

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.

Keywords

Allergy Bovine beta-lactoglobulin Anaphylactic reaction Bacillus subtilis Proteolytic activity 

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Compliance with ethics requirements

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

References

  1. 1.
    Platts-Mills TAE (2015) J Allergy Clin Immunol 136:3–13CrossRefGoogle Scholar
  2. 2.
    Hochwallner H, Schulmeister U, Swoboda I, Spitzauer S, Valenta R (2014) Methods 66:22–33CrossRefGoogle Scholar
  3. 3.
    Virta LJ, Ashorn M, Kolho KL (2013) J Pediatr Gastroenterol Nutr 56:649–651CrossRefGoogle Scholar
  4. 4.
    Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2010) Gastroenterol 139:1844–1854CrossRefGoogle Scholar
  5. 5.
    Levy R, Borenstein E (2014) Gut Microbes 5:37–41CrossRefGoogle Scholar
  6. 6.
    Jackson M, Jeffery IB, Beaumont M, Bell JT, Clark AG, Ley RE, O’Toole PW, Spector TD, Steves CJ (2016) Genome Med 8:8CrossRefGoogle Scholar
  7. 7.
    Ivakhnenko ES (2013) Nian’kovskiĭ SL. Georgian Med News 219:46–52Google Scholar
  8. 8.
    Martin CR, Ling PR, Blackburn GL (2016) Nutrients 8:279–289CrossRefGoogle Scholar
  9. 9.
    Cutting SM (2011) Food Microbiol 28:214–220CrossRefGoogle Scholar
  10. 10.
    Hong HA, Le Duc H, Cutting SM (2005) FEMS Microbiol Rev 29:813–835CrossRefGoogle Scholar
  11. 11.
    Tompkins TA, Xu X, Ahmarani J (2010) Benef Microbes 1:93–106CrossRefGoogle Scholar
  12. 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 Google Scholar
  13. 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 CrossRefGoogle Scholar
  14. 14.
    Zhu F, Cai J, Wu X, Huang J, Huang L, Zhud J, Zheng Q, Cen P, Xu Z (2013) J Biotechnol 164:67–74CrossRefGoogle Scholar
  15. 15.
    Xu Z, Feng X, Zhang D, Tang B, Lei P, Liang J, Xu H (2014) Bioresour Technol 155:8–14CrossRefGoogle Scholar
  16. 16.
    Fu J, Wang Z, Chen T, Liu W, Shi T, Wang G, Tang Y, Zhao X (2014) Biotechnol Bioeng 111:2126–2131CrossRefGoogle Scholar
  17. 17.
    Zhang X, Zhang R, Bao T, Rao Z, Yang T, Xu M, Xu Z, Li H, Yang S (2014) Metab Eng 23:34–41CrossRefGoogle Scholar
  18. 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 6:587–590Google Scholar
  19. 19.
    El-Ghaish S, Dalgalarrondo M, Choiset Y, Sitohy M, Ivanova I, Haertlé T, Chobert J-M (2010) Eur Food Res Technol 230:635–643CrossRefGoogle Scholar
  20. 20.
    Laemmli UK (1970) Nature 227:680–685CrossRefGoogle Scholar
  21. 21.
    Doi E, Shibata D, Matoba T (1981) Anal Biochem 118:173–184CrossRefGoogle Scholar
  22. 22.
    Zellal D, Kaddouri H, Grar H, Belarbi H, Kheroua O, Saidi D (2011) Food Agric Immunol 22:355–363CrossRefGoogle Scholar
  23. 23.
    Adel-Patient K, Créminon C, Bernard H, Clément G, Négroni L, Frobert Y, Grassi J, Wal JM, Chatel JM (2000) J Immunol Methods 235:21–32CrossRefGoogle Scholar
  24. 24.
    Negaoui H, Kaddouri H, Kheroua O, Saidi D (2009) Am J Immunol 5:56–60CrossRefGoogle Scholar
  25. 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 241:393–398CrossRefGoogle Scholar
  26. 26.
    Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA (1999) J Allergy Clin Immunol 103:206–214CrossRefGoogle Scholar
  27. 27.
    Priest F (1977) Bacteriol Rev 41:711–753Google Scholar
  28. 28.
    Schallmey M, Singh A, Ward OP (2004) Can J Microbiol 50:1–17CrossRefGoogle Scholar
  29. 29.
    Li W, Zhou X, Lu P (2004) Res Microbiol 155:605–610CrossRefGoogle Scholar
  30. 30.
    Nijland R, Kuipers O (2008) Recent Pat Biotechnol 2:79–87CrossRefGoogle Scholar
  31. 31.
    Chantawannakul P, Oncharoen A, Klanbut K, Chukeatirote E, Lumyong S (2002) Sci Asia 28:241–245CrossRefGoogle Scholar
  32. 32.
    Gaustevora A, Braikova D, Christov P, Tishinov K, Tonkova EV, Haertlé T, Nedkov P (2005) Lett Appl Microbiol 40:335–340CrossRefGoogle Scholar
  33. 33.
    Kamoun AS, Haddar A, Ali NEH, Basma FG, Kanoun S, Nasri M (2008) Microbiol Res 163:299–306CrossRefGoogle Scholar
  34. 34.
    Kramer JM, Gilbert RJ (1989) In: Doyle MP (ed) Foodborne bacterial pathogens. Marcel Dekker, New YorkGoogle Scholar
  35. 35.
    Denner WHB, Gillanders TGE (1996) In: Godfrey T, West S (eds) The Macmillan Press Ltd, 2nd edn. Basingstoke, UKGoogle Scholar
  36. 36.
    Zhou Z, Song Y, Mao C, Srivastava KD, Liu C, Yang N, Li XM (2015) Clin Immunol 135(2):AB29Google Scholar
  37. 37.
    Huang JM, La Ragione RM, Nunez A, Cutting SM (2008) FEMS Immunol Med Microbiol 53:195–203CrossRefGoogle Scholar
  38. 38.
    Mehrad B, Standiford TJ (1999) Immunol Res 20:15–27CrossRefGoogle Scholar
  39. 39.
    Sadler AJ, Williams BR (2008) Nat Rev Immunol 8:559–568CrossRefGoogle Scholar
  40. 40.
    Michail S (2009) Allergy Asthma Clin Immunol 5:5CrossRefGoogle Scholar
  41. 41.
    Tang RB, Chen SJ (2001) Ann Allergy Asthma Immunol 86:314–317CrossRefGoogle Scholar
  42. 42.
    Hu CH, Gu LY, Luan ZS, Song J, Zhu K (2012) Anim Feed Sci Technol 177:108–115CrossRefGoogle Scholar
  43. 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 318:683–690Google Scholar
  44. 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 5:356–364Google Scholar
  45. 45.
    Crowe SE, Perdue MH (1992) Gastroenterol 103:1075–1095CrossRefGoogle Scholar
  46. 46.
    Schiffer C, Lalanne AI, Cassard L, Mancardi DA, Malbec O, Bruhns P, Dif F, Daeron M (2011) J Immunol 187:2646–2655CrossRefGoogle Scholar
  47. 47.
    Forsythe P, Wang B, Khambati I, Kunze WA (2012) PLoS One 7:e41234CrossRefGoogle Scholar
  48. 48.
    Oksaharju A, Kankainen M, Kekkonen RA, Lindstedt KA, Kovanen PT, Korpela R, Miettinen M (2011) World J Gastroenterol 17:750–759CrossRefGoogle Scholar
  49. 49.
    Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, DeSimone C (2001) Gastroenterol 121:580–591CrossRefGoogle Scholar
  50. 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–G1034CrossRefGoogle Scholar
  51. 51.
    Sanchez B, Arias S, Chaignepain S, Denayrolles M, Schmitter JM, Bressollier P, Urdaci MC (2009) Microbiol 155:1708–1716CrossRefGoogle Scholar
  52. 52.
    Fujiya M, Musc MW, Nakagawa Y, Hu S, Alverdy J, Kohgo Y, Schneewind O, Jabri B, Chang EB (2007) Cell Host Microbe 1:299–308CrossRefGoogle Scholar
  53. 53.
    Hosoi T, Hirose R, Saegusa S, Ametani A, Kiuchi K, Kaminogawa S (2003) Int J Food Microbiol 82:255–264CrossRefGoogle Scholar
  54. 54.
    Urdaci MC, Bressollier P, Pinchuk I (2004) J Clin Gastroenterol 38:S86–S90CrossRefGoogle Scholar
  55. 55.
    Fiorini G, Cimminiello C, Chianese R, Visconti GP, Cova D, Uberti T, Gibelli A (1985) Chemioterapia 4:310–312Google Scholar
  56. 56.
    Le Duc H, Hong HA, Barbosa TM, Henriques AO, Cutting SM (2004) Appl Environ Microbiol 70:2161–2171CrossRefGoogle Scholar
  57. 57.
    Hong HA, Khaneja R, Tam NM, Cazzato A, Tan S, Urdaci M, Brisson A, Gasbarrini A, Barnes I, Cutting SM (2009) Res Microbiol 160:134–143CrossRefGoogle Scholar
  58. 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 8:4CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Wafaa Dib
    • 1
    • 2
    Email author
  • Hadria Grar
    • 1
    • 3
  • Hanane Gourine
    • 1
  • Kamel Eddine El Mecherfi
    • 1
  • Hanane Negaoui
    • 1
  • Vanessa Biscola
    • 4
  • Hanane Kaddouri
    • 1
  • Jean-Marc Chobert
    • 5
  • Thomas Haertlé
    • 5
    • 6
    • 7
  • Djamel Saidi
    • 1
  • Omar Kheroua
    • 1
  1. 1.Laboratory of the Physiology of Nutrition and Food Safety, Department of Biology, Faculty of Natural and Life ScienceUniversity of Oran 1, Ahmed Ben BellaOranAlgeria
  2. 2.Department of Biotechnology, Faculty of Natural and Life ScienceUniversity of Science and Technology Mohamed BoudiafOranAlgeria
  3. 3.Department of Biology, Faculty of ScienceUniversity of MostaganemMostaganemAlgeria
  4. 4.Department of Food and Experimental Nutrition, Faculty of Pharmaceutical SciencesUniversity of São PauloSão PauloBrazil
  5. 5.UR 1268, Biopolymères Interactions Assemblages, INRANantesFrance
  6. 6.Department of Animal Nutrition and Feed ManagementPoznan University of Life SciencesPoznańPoland
  7. 7.Institute of Biochemistry and BiophysicsUniversity of TeheranTehranIran

Personalised recommendations