A specific mixture of Fructo-Oligosaccharides and Bifidobacterium breve M-16V facilitates partial non-responsiveness to whey protein in mice orally exposed to β-lactoglobulin-derived peptides

Frontiers in Immunology

Volumn 7, Issue JAN, 2017, Pages

  Kostadinova, Atanaska I ^a,b   Meulenbroek, Laura A P M ^b   van Esch, Betty C A M ^a,b   Hofman, Gerard A ^a   Garssen, Johan ^a,b   Willemsen, Linette E M ^a   Knippels, Léon M J ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b DANONE NUTRICIA RESEARCH   (Netherlands)

Author keywords

Acute allergic skin response; Dietary interventions; Food allergy; Mouse models; Oral tolerance; Peptides; Prevention; T cells

Indexed keywords

BETA LACTOGLOBULIN; CHOLERA TOXIN; FRUCTOSE OLIGOSACCHARIDE; GAMMA INTERFERON; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 5; SHORT CHAIN FATTY ACID; SYNBIOTIC AGENT; WHEY PROTEIN;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIFIDOBACTERIUM BREVE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIETARY SUPPLEMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; LAMINA PROPRIA; MILK ALLERGY; MOUSE; NONHUMAN; PHENOTYPE; STIMULATION; T LYMPHOCYTE;

EID: 85012045729     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00673     Document Type: Article

References (51)

1. Skripak JM, Matsui EC, Mudd K, Wood RA. The natural history of IgE-mediated cow's milk allergy. J Allergy Clin Immunol (2007) 120(5):1172-7. doi: 10.1016/j.jaci.2007.08.023.
2. Ahrens B, Sampson HA, Beyer K. Adverse reactions to food. In: Wahn U, Sampson HA, editors. Allergy, Immunity and Tolerance in Early Childhood: The First Steps of the Atopic March. San Diego, Waltham, London, Oxford: Academic Press (2015).
3. Joneja JM. Infant food allergy: where are we now? JPEN J Parenter Enteral Nutr (2012) 36(1 Suppl):49S-55S. doi:10.1177/0148607111420155.
4. Dello II, Verga MC. Sudden loss of cow's milk tolerance in a long-sensitized patient. Eur Ann Allergy Clin Immunol (2012) 44(4):172-4.
5. Chase MW. Inhibition of experimental drug allergy by prior feeding of the sensitizing agent. Proc Soc Exp Biol Med (1946) 61:257-9. doi:10.3181/00379727-61-15294P.
6. Mowat AM, Strobel S, Drummond HE, Ferguson A. Immunological responses to fed protein antigens in mice. I. Reversal of oral tolerance to ovalbumin by cyclophosphamide. Immunology (1982) 45(1):105-13.
7. Prescott SL, Smith P, Tang M, Palmer DJ, Sinn J, Huntley SJ, et al. The importance of early complementary feeding in the development of oral tolerance: concerns and controversies. Pediatr Allergy Immunol (2008) 19(5):375-80. doi:10.1111/j.1399-3038.2008.00718.x.
8. Du Toit G, Katz Y, Sasieni P, Mesher D, Maleki SJ, Fisher HR, et al. Early consumption of peanuts in infancy is associated with a low prevalence of peanut allergy. J Allergy Clin Immunol (2008) 122(5):984-91. doi:10.1016/j.jaci.2008.08.039.
9. Du Toit G, Roberts G, Sayre PH, Bahnson HT, Radulovic S, Santos AF, et al. Randomized trial of peanut consumption in infants at risk for peanut allergy. N Engl J Med (2015) 372(9):803-13. doi:10.1056/NEJMoa1414850.
10. van Esch BC, Schouten B, de Kivit S, Hofman GA, Knippels LM, Willemsen LE, et al. Oral tolerance induction by partially hydrolyzed whey protein in mice is associated with enhanced numbers of Foxp3+ regulatory T-cells in the mesenteric lymph nodes. Pediatr Allergy Immunol (2011) 22(8):820-6. doi:10.1111/j.1399-3038.2011.01205.x.
11. Hoyne GF, Jarnicki AG, Thomas WR, Lamb JR. Characterization of the specificity and duration of T cell tolerance to intranasally administered peptides in mice: a role for intramolecular epitope suppression. Int Immunol (1997) 9(8):1165-73. doi:10.1093/intimm/9.8.1165.
12. Pecquet S, Bovetto L, Maynard F, Fritsche R. Peptides obtained by tryptic hydrolysis of bovine beta-lactoglobulin induce specific oral tolerance in mice. J Allergy Clin Immunol (2000) 105(3):514-21. doi:10.1067/mai.2000.103049.
13. Bogh KL, Barkholt V, Madsen CB. The sensitising capacity of intact beta-lactoglobulin is reduced by co-administration with digested beta-lactoglobulin. Int Arch Allergy Immunol (2013) 161(1):21-36. doi:10.1159/000343042.
14. Meulenbroek LA, van Esch BC, Hofman GA, den Hartog Jager CF, Nauta AJ, Willemsen LE, et al. Oral treatment with beta-lactoglobulin peptides prevents clinical symptoms in a mouse model for cow's milk allergy. Pediatr Allergy Immunol (2013) 24(7):656-64. doi:10.1111/pai.12120.
15. Gourbeyre P, Denery S, Bodinier M. Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol (2011) 89(5):685-95. doi:10.1189/jlb.1109753.
16. Arslanoglu S, Moro GE, Schmitt J, Tandoi L, Rizzardi S, Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J Nutr (2008) 138(6):1091-5.
17. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child (2006) 91(10):814-9. doi:10.1136/adc.2006.098251.
18. Moro G, Minoli I, Mosca M, Fanaro S, Jelinek J, Stahl B, et al. Dosage-related bifidogenic effects of galacto-and fructooligosaccharides in formula-fed term infants. J Pediatr Gastroenterol Nutr (2002) 34(3):291-5. doi:10.1097/00005176-200203000-00014.
19. Nauta AJ, Garssen J. Evidence-based benefits of specific mixtures of non-digestible oligosaccharides on the immune system. Carbohydr Polym (2013) 93(1):263-5. doi:10.1016/j.carbpol.2012.02.021.
20. Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol (2001) 108(4):516-20. doi:10.1067/mai.2001.118130.
21. Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, et al. Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep (2016) 15(12):2809-24. doi:10.1016/j.celrep.2016.05.047.
22. Hidaka H, Eida T, Takizawa T, Tokunaga T, Tashiro Y. Effects of fructooligosaccharides on intestinal flora and human health. Bifidobact Microflora (1986) 5(1):37-50. doi:10.12938/bifidus1982.5.1_37.
23. Macfarlane GT, Cummings JH. Probiotics and prebiotics: can regulating the activities of intestinal bacteria benefit health? BMJ (1999) 318(7189):999-1003. doi:10.1136/bmj.318.7189.999.
24. Schouten B, van Esch BC, Hofman GA, Boon L, Knippels LM, Willemsen LE, et al. Oligosaccharide-induced whey-specific CD25(+) regulatory T-cells are involved in the suppression of cow milk allergy in mice. J Nutr (2010) 140(4):835-41. doi:10.3945/jn.109.116061.
25. Vos AP, van Esch BC, Stahl B, M'Rabet L, Folkerts G, Nijkamp FP, et al. Dietary supplementation with specific oligosaccharide mixtures decreases parameters of allergic asthma in mice. Int Immunopharmacol (2007) 7(12):1582-7. doi:10.1016/j.intimp.2007.07.024.
26. Hougee S, Vriesema AJ, Wijering SC, Knippels LM, Folkerts G, Nijkamp FP, et al. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int Arch Allergy Immunol (2010) 151(2):107-17. doi:10.1159/000236000.
27. Inoue Y, Iwabuchi N, Xiao J-ZZ, Yaeshima T, Iwatsuki K. Suppressive effects of Bifidobacterium breve strain M-16V on T-helper type 2 immune responses in a murine model. Biol Pharm Bull (2009) 32(4):760-3. doi:10.1248/bpb.32.760.
28. Taniuchi S, Hattori K, Yamamoto A, Sasai M, Hatano Y, Kojima T, et al. Administration of Bifidobacterium to infants with atopic dermatitis: changes in fecal microflora and clinical symptoms. J Appl Res (2005) 5(2):387-96.
29. Schouten B, van Esch BC, Hofman GA, van Doorn SA, Knol J, Nauta AJ, et al. Cow milk allergy symptoms are reduced in mice fed dietary synbiotics during oral sensitization with whey. J Nutr (2009) 139(7):1398-403. doi:10.3945/jn.109.108514.
30. van Esch BC, Abbring S, Diks MA, Dingjan GM, Harthoorn LF, Vos AP, et al. Post-sensitization administration of non-digestible oligosaccharides and Bifidobacterium breve M-16V reduces allergic symptoms in mice. Immun Inflamm Dis (2016) 4(2):155-65. doi:10.1002/iid3.101.
31. Verheijden KA, Willemsen LE, Braber S, Leusink-Muis T, Jeurink PV, Garssen J, et al. The development of allergic inflammation in a murine house dust mite asthma model is suppressed by synbiotic mixtures of non-digestible oligosaccharides and Bifidobacterium breve M-16V. Eur J Nutr (2016) 55(3):1141-51. doi:10.1007/s00394-015-0928-8.
32. Burks AW, Harthoorn LF, Van Ampting MT, Oude Nijhuis MM, Langford JE, Wopereis H, et al. Synbiotics-supplemented amino acid-based formula supports adequate growth in cow's milk allergic infants. Pediatr Allergy Immunol (2015) 26(4):316-22. doi:10.1111/pai.12390.
33. Rigo-Adrover MD, Franch A, Castell M, Perez-Cano FJ. Preclinical immunomodulation by the probiotic Bifidobacterium breve M-16V in early life. PLoS One (2016) 11(11):e0166082. doi:10.1371/journal.pone.0166082.
34. Fujii T, Ohtsuka Y, Lee T, Kudo T, Shoji H, Sato H, et al. Bifidobacterium breve enhances transforming growth factor beta1 signaling by regulating Smad7 expression in preterm infants. J Pediatr Gastroenterol Nutr (2006) 43(1):83-8. doi:10.1097/01.mpg.0000228100.04702.f8.
35. Boesten RJ, Schuren FH, Willemsen LE, Vriesema A, Knol J, De Vos WM. Bifidobacterium breve-HT-29 cell line interaction: modulation of TNF-alpha induced gene expression. Benef Microbes (2011) 2(2):115-28. doi:10.3920/bm2011.0005.
36. de Theije CG, Wopereis H, Ramadan M, van Eijndthoven T, Lambert J, Knol J, et al. Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain Behav Immun (2014) 37:197-206. doi:10.1016/j.bbi.2013.12.005.
37. Mousallem T, Burks AW. Immunology in the clinic review series; focus on allergies: immunotherapy for food allergy. Clin Exp Immunol (2012) 167(1):26-31. doi:10.1111/j.1365-2249.2011.04499.x.
38. Coombes JL, Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol (2008) 8(6):435-46. doi:10.1038/nri2335.
39. Fujimoto K, Karuppuchamy T, Takemura N, Shimohigoshi M, Machida T, Haseda Y, et al. A new subset of CD103+CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol (2011) 186(11):6287-95. doi:10.4049/jimmunol.1004036.
40. van den Elsen LW, van Esch BC, Hofman GA, Kant J, van de Heijning BJ, Garssen J, et al. Dietary long chain n-3 polyunsaturated fatty acids prevent allergic sensitization to cow's milk protein in mice. Clin Exp Allergy (2013) 43(7):798-810. doi:10.1111/cea.12111.
41. Persson EK, Scott CL, Mowat AM, Agace WW. Dendritic cell subsets in the intestinal lamina propria: ontogeny and function. Eur J Immunol (2013) 43(12):3098-107. doi:10.1002/eji.201343740.
42. Janssen EM, van Oosterhout AJ, van Rensen AJ, van Eden W, Nijkamp FP, Wauben MH. Modulation of Th2 responses by peptide analogues in a murine model of allergic asthma: amelioration or deterioration of the disease process depends on the Th1 or Th2 skewing characteristics of the therapeutic peptide. J Immunol (2000) 164(2):580-8. doi:10.4049/jimmunol.164.2.580.
43. Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S, Helm K, et al. Colon microflora in infants fed formula with galacto-and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr (2005) 40(1):36-42. doi:10.1097/00005176-200501000-00007.
44. Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med (2014) 20(2):159-66. doi:10.1038/nm.3444.
45. Kulis M, Macqueen I, Li Y, Guo R, Zhong XP, Burks AW. Pepsinized cashew proteins are hypoallergenic and immunogenic and provide effective immunotherapy in mice with cashew allergy. J Allergy Clin Immunol (2012) 130(3):716-23. doi:10.1016/j.jaci.2012.05.044.
46. Weiner HL. Oral tolerance: immune mechanisms and the generation of Th3-type TGF-beta-secreting regulatory cells. Microbes Infect (2001) 3(11):947-54. doi:10.1016/S1286-4579(01)01456-3.
47. Faria AM, Weiner HL. Oral tolerance. Immunol Rev (2005) 206:232-59. doi:10.1111/j.0105-2896.2005.00280.x.
48. Hacini-Rachinel F, Vissers YM, Doucet-Ladeveze R, Blanchard C, Demont A, Perrot M, et al. Low-allergenic hydrolyzed egg induces oral tolerance in mice. Int Arch Allergy Immunol (2014) 164(1):64-73. doi:10.1159/000363110.
49. Perrier C, Thierry AC, Mercenier A, Corthesy B. Allergen-specific antibody and cytokine responses, mast cell reactivity and intestinal permeability upon oral challenge of sensitized and tolerized mice. Clin Exp Allergy (2010) 40(1):153-62. doi:10.1111/j.1365-2222.2009.03329.x.
50. Gaur A, Wiers B, Liu A, Rothbard J, Fathman CG. Amelioration of autoimmune encephalomyelitis by myelin basic protein synthetic peptide-induced anergy. Science (1992) 258(5087):1491-4. doi:10.1126/science.1279812.
51. Liu GY, Wraith DC. Affinity for class II MHC determines the extent to which soluble peptides tolerize autoreactive T cells in naive and primed adult mice-implications for autoimmunity. Int Immunol (1995) 7(8):1255-63. doi:10.1093/intimm/7.8.1255.