The Combination of 2'-Fucosyllactose with Short-Chain Galacto-Oligosaccharides and Long-Chain Fructo-Oligosaccharides that Enhance Influenza Vaccine Responses Is Associated with Mucosal Immune Regulation in Mice

J Nutr. 2019 May 1;149(5):856-869. doi: 10.1093/jn/nxz006.

Abstract

Background: A critical role for host-microbe interactions and establishment of vaccine responses has been postulated. Human milk oligosaccharides, of which 2'-fucosyllactose (2'FL) is the most prevalent, are known to alter host-associated microbial communities and play a critical role in the immunologic development of breastfed infants.

Objectives: Dietary supplementation with a combination of 2'FL and prebiotic short-chain (sc) galacto-oligosaccharides (GOS) and long-chain (lc) fructo-oligosaccharides (FOS) was employed to examine human milk oligosaccharide effects on immune responsiveness, within a murine influenza vaccination model.

Methods: Female mice (6 wk old, C57Bl/6JOlaHsd) were fed either control diet (CON) or scGOS/lcFOS/2'FL-containing diet (GF2F) for 45 d. After starting dietary intervention (day 14), mice received a primary influenza vaccination (day 0) followed by a booster vaccination (day 21), after which ear challenges were conducted to measure vaccine-specific delayed type hypersensitivity (DTH). Serum immunoglobulin (Ig) levels, fecal and cecal microbial community structure, short-chain fatty acids, host intestinal gene expression and cellular responses in the mesenteric lymph nodes (MLNs) were also measured.

Results: Relative to CON, mice fed the GF2F diet had increased influenza vaccine-specific DTH responses (79.3%; P < 0.01), higher levels of both IgG1 (3.2-fold; P < 0.05) and IgG2a (1.2-fold; P < 0.05) in serum, and greater percentages of activated B cells (0.3%; P < 0.05), regulatory T cells (1.64%; P < 0.05), and T-helper 1 cells (2.2%; P < 0.05) in their MLNs. GF2F-fed mice had elevated cecal butyric (P < 0.05) and propionic (P < 0.05) acid levels relative to CON, which correlated to DTH responses (R2 = 0.22; P = 0.05 and R2 = 0.39; P < 0.01, respectively). Specific fecal microbial taxa altered in GF2F diet fed mice relative to CON were significantly correlated with the DTH response and IgG2a level increases.

Conclusions: Dietary GF2F improved influenza vaccine-specific T-helper 1 responses and B cell activation in MLNs and enhanced systemic IgG1 and IgG2a concentrations in mice. These immunologic changes are correlated with microbial community structure and metabolites.

Keywords: 2′-fucosyllactose; gut microbiota; influenza vaccine; oligosaccharides; short-chain fatty acids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes
  • Cecum / metabolism
  • Cecum / microbiology
  • Colon / metabolism
  • Colon / microbiology
  • Feces / microbiology
  • Female
  • Fructose / pharmacology
  • Fructose / therapeutic use
  • Galactose / pharmacology
  • Galactose / therapeutic use
  • Humans
  • Immunoglobulin G / blood
  • Immunologic Factors / pharmacology
  • Immunologic Factors / therapeutic use
  • Influenza Vaccines*
  • Influenza, Human / immunology
  • Influenza, Human / prevention & control*
  • Mice, Inbred C57BL
  • Milk, Human / chemistry*
  • Mucous Membrane / drug effects*
  • Mucous Membrane / immunology
  • Oligosaccharides / pharmacology
  • Oligosaccharides / therapeutic use*
  • Prebiotics*
  • Th1 Cells
  • Trisaccharides / pharmacology
  • Trisaccharides / therapeutic use*
  • Vaccination

Substances

  • Immunoglobulin G
  • Immunologic Factors
  • Influenza Vaccines
  • Oligosaccharides
  • Prebiotics
  • Trisaccharides
  • Fructose
  • Galactose
  • 2'-fucosyllactose