Human Milk Oligosaccharides in Combination with Galacto- and Long-Chain Fructo-Oligosaccharides Enhance Vaccination Efficacy in a Murine Influenza Vaccination Model
Abstract
:1. Introduction
2. Materials and Methods
2.1. Mice
2.2. Diet
2.3. Vaccination Protocol
2.4. Antigen-Specific Delayed-Type Hypersensitivity
2.5. Vaccine-Specific Immunoglobulin (Ig) Analysis in Serum
2.6. Splenocytes Isolation
2.7. Flow Cytometric Analysis of Splenocytes
2.8. Development of Bone Marrow-Derived Dendritic Cells
2.9. Splenocyte Restimulation Using Vaccine-Loaded BMDCs Ex Vivo
2.10. Statistical Analysis
3. Results
3.1. The Combination of GOS/lcFOS and HMOS Enhances the Delayed-Type Hypersensitivity Response
3.2. Influvac-Specific Immunoglobulins Are Increased after Oligosaccharide Intervention
3.3. Dietary HMOS and GOS/lcFOS Enhances Splenic Memory B Cells
3.4. The Combination of GOS/lcFOS and HMOS Increases Activation of Splenic T Helper 1 Cells
3.5. The Combination of GOS/lcFOS and HMOS Increases the Production of IFN-γ in Splenocytes-DCs when Co-Cultured Ex Vivo
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Niewiesk, S. Maternal antibodies: Clinical significance, mechanism of interference with immune responses, and possible vaccination strategies. Front. Immunol. 2014, 5, 446. [Google Scholar] [CrossRef] [PubMed]
- Siegrist, C.-A. The challenges of vaccine responses in early life: Selected examples. J. Comp. Pathol. 2007, 137, S4–S9. [Google Scholar] [CrossRef]
- Basha, S.; Surendran, N.; Pichichero, M. Immune responses in neonates. Expert Rev. Clin. Immunol. 2014, 10, 1171–1184. [Google Scholar] [CrossRef] [PubMed]
- Levy, O. Innate Immunity of the Newborn: Basic Mechanisms and Clinical Correlates. Nat. Rev. Immunol. 2007, 7, 379–390. [Google Scholar] [CrossRef]
- Adkins, B.; Leclerc, C.; Marshall-Clarke, S. Neonatal Adaptive Immunity Comes of Age. Nat. Rev. Immunol. 2004, 4, 553–564. [Google Scholar] [CrossRef]
- Mohr, E.; Siegrist, C.-A. Vaccination in early life: Standing up to the challenges. Curr. Opin. Immunol. 2016, 41, 1–8. [Google Scholar] [CrossRef]
- Dowling, D.J.; Levy, O. Ontogeny of early life immunity. Trends Immunol. 2014, 35, 299–310. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, A.; Medzhitov, R. Control of adaptive immunity by the innate immune system. Nat. Immunol. 2015, 16, 343–353. [Google Scholar] [CrossRef] [PubMed]
- Sebina, I.; Pepper, M. Humoral immune responses to infection: Common mechanisms and unique strategies to combat pathogen immune evasion tactics. Curr. Opin. Immunol. 2018, 51, 46–54. [Google Scholar] [CrossRef]
- Lambert, P.-H.; Liu, M.; Siegrist, C.-A. Can successful vaccines teach us how to induce efficient protective immune responses? Nat. Med. 2005, 11 (Suppl. S4), S54–S62. [Google Scholar] [CrossRef]
- Falahi, S.; Kenarkoohi, A. Host factors and vaccine efficacy: Implications for COVID-19 vaccines. J. Med. Virol. 2022, 94, 1330–1335. [Google Scholar] [CrossRef] [PubMed]
- Reyman, M.; van Houten, M.A.; van Baarle, D.; Bosch, A.A.; Man, W.H.; Chu, M.L.J.; Arp, K.; Watson, R.L.; Sanders, E.A.; Fuentes, S. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat. Commun. 2019, 10, 4997. [Google Scholar] [CrossRef]
- Jordan, A.; Carding, S.R.; Hall, L.J. The early-life gut microbiome and vaccine efficacy. Lancet Microbe 2022, 3, e787–e794. [Google Scholar] [CrossRef] [PubMed]
- Collins, N.; Belkaid, Y. Do the microbiota influence vaccines and protective immunity to pathogens? Engaging our endogenous adjuvants. Cold Spring Harb. Perspect. Biol. 2018, 10, a028860. [Google Scholar] [CrossRef]
- Oh, J.Z.; Ravindran, R.; Chassaing, B.; Carvalho, F.A.; Maddur, M.S.; Bower, M.; Hakimpour, P.; Gill, K.P.; Nakaya, H.I.; Yarovinsky, F. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 2014, 41, 478–492. [Google Scholar] [CrossRef] [PubMed]
- Ponziani, F.R.; Coppola, G.; Rio, P.; Caldarelli, M.; Borriello, R.; Gambassi, G.; Gasbarrini, A.; Cianci, R. Factors influencing microbiota in modulating vaccine immune response: A long way to go. Vaccines 2023, 11, 1609. [Google Scholar] [CrossRef]
- Rousseaux, A.; Brosseau, C.; Bodinier, M. Immunomodulation of B lymphocytes by prebiotics, probiotics and synbiotics: Application in pathologies. Nutrients 2023, 15, 269. [Google Scholar] [CrossRef]
- Sprenger, N.; Tytgat, H.L.; Binia, A.; Austin, S.; Singhal, A. Biology of human milk oligosaccharide: From basic science to clinical evidence. J. Hum. Nutr. Diet. 2022, 35, 280–299. [Google Scholar] [CrossRef]
- Moubareck, C.A. Human milk microbiota and oligosaccharides: A glimpse into benefits, diversity, and correlations. Nutrients 2021, 13, 1123. [Google Scholar] [CrossRef]
- Hill, D.R.; Chow, J.M.; Buck, R.H. Multifunctional benefits of prevalent HMOs: Implications for infant health. Nutrients 2021, 13, 3364. [Google Scholar] [CrossRef]
- Perdijk, O.; Van Baarlen, P.; Fernandez-Gutierrez, M.M.; Van den Brink, E.; Schuren, F.H.; Brugman, S.; Savelkoul, H.F.; Kleerebezem, M.; Van Neerven, R.J. Sialyllactose and galactooligosaccharides promote epithelial barrier functioning and distinctly modulate microbiota composition and short chain fatty acid production in vitro. Front. Immunol. 2019, 10, 94. [Google Scholar] [CrossRef] [PubMed]
- Rosa, F.; Sharma, A.K.; Gurung, M.; Casero, D.; Matazel, K.; Bode, L.; Simecka, C.; Elolimy, A.A.; Tripp, P.; Randolph, C. Human milk oligosaccharide impact cellular and inflammatory gene expression and immune response. Front. Immunol. 2022, 13, 907529. [Google Scholar] [CrossRef] [PubMed]
- Fabiano, V.; Indrio, F.; Verduci, E.; Calcaterra, V.; Pop, T.L.; Mari, A.; Zuccotti, G.V.; Cullu Cokugras, F.; Pettoello-Mantovani, M.; Goulet, O. Term infant formulas influencing gut microbiota: An overview. Nutrients 2021, 13, 4200. [Google Scholar] [CrossRef]
- Salminen, S.; Stahl, B.; Vinderola, G.; Szajewska, H. Infant formula supplemented with biotics: Current knowledge and future perspectives. Nutrients 2020, 12, 1952. [Google Scholar] [CrossRef] [PubMed]
- Ayechu-Muruzabal, V.; van de Kaa, M.; Mukherjee, R.; Garssen, J.; Stahl, B.; Pieters, R.J.; Van’T Land, B.; Kraneveld, A.D.; Willemsen, L.E. Modulation of the epithelial-immune cell crosstalk and related galectin secretion by DP3-5 galacto-oligosaccharide and β-3′ galactosyllactose. Biomolecules 2022, 12, 384. [Google Scholar] [CrossRef]
- Reeves, P.G. Components of the AIN-93 diets as improvements in the AIN-76A diet. J. Nutr. 1997, 127, 838S–841S. [Google Scholar] [CrossRef]
- Coulier, L.; Timmermans, J.; Bas, R.; Van Den Dool, R.; Haaksman, I.; Klarenbeek, B.; Slaghek, T.; Van Dongen, W. In-depth characterization of prebiotic galacto-oligosaccharide by a combination of analytical techniques. J. Agric. Food Chem. 2009, 57, 8488–8495. [Google Scholar] [CrossRef]
- Kittibunchakul, S.; Van Leeuwen, S.S.; Dijkhuizen, L.; Haltrich, D.; Nguyen, T.-H. Structural comparison of different galacto-oligosaccharide mixtures formed by β-galactosidases from lactic acid bacteria and bifidobacteria. J. Agric. Food Chem. 2020, 68, 4437–4446. [Google Scholar] [CrossRef]
- Van Leeuwen, S.S.; Kuipers, B.J.; Dijkhuizen, L.; Kamerling, J.P. 1H NMR analysis of the lactose/β-galactosidase-derived galacto-oligosaccharide components of Vivinal® GOS up to DP5. Carbohydr. Res. 2014, 400, 59–73. [Google Scholar] [CrossRef]
- Vonk, M.M.; Blokhuis, B.R.; Diks, M.A.; Wagenaar, L.; Smit, J.J.; Pieters, R.H.; Garssen, J.; Knippels, L.M.; van Esch, B.C. Butyrate enhances desensitization induced by oral immunotherapy in cow’s milk allergic mice. Mediat. Inflamm. 2019, 2019, 9062537. [Google Scholar] [CrossRef]
- Xiao, L.; Leusink-Muis, T.; Kettelarij, N.; Van Ark, I.; Blijenberg, B.; Hesen, N.A.; Stahl, B.; Overbeek, S.A.; Garssen, J.; Folkerts, G. Human milk oligosaccharide 2′-fucosyllactose improves innate and adaptive immunity in an influenza-specific murine vaccination model. Front. Immunol. 2018, 9, 452. [Google Scholar] [CrossRef]
- Seyed Toutounchi, N.; Braber, S.; van’t Land, B.; Thijssen, S.; Garssen, J.; Kraneveld, A.D.; Folkerts, G.; Hogenkamp, A. Exposure to deoxynivalenol during pregnancy and lactation enhances food allergy and reduces vaccine responsiveness in the offspring in a mouse model. Front. Immunol. 2021, 12, 797152. [Google Scholar] [CrossRef]
- Van Vlies, N.; Hogenkamp, A.; Fear, A.; Van Esch, B.; Oosting, A.; Van de Heijning, B.; Van Der Beek, E.; Calder, P.; Garssen, J. Perinatal programming of murine immune responses by polyunsaturated fatty acids. J. Dev. Orig. Health Dis. 2011, 2, 112–123. [Google Scholar] [CrossRef]
- Albers, R.; Bourdet-Sicard, R.; Braun, D.; Calder, P.C.; Herz, U.; Lambert, C.; Lenoir-Wijnkoop, I.; Meheust, A.; Ouwehand, A.; Phothirath, P. Monitoring immune modulation by nutrition in the general population: Identifying and substantiating effects on human health. Br. J. Nutr. 2013, 110, S1–S30. [Google Scholar] [CrossRef]
- Lynn, M.A.; Tumes, D.J.; Choo, J.M.; Sribnaia, A.; Blake, S.J.; Leong, L.E.X.; Young, G.P.; Marshall, H.S.; Wesselingh, S.L.; Rogers, G.B. Early-life antibiotic-driven dysbiosis leads to dysregulated vaccine immune responses in mice. Cell Host Microbe 2018, 23, 653–660.e5. [Google Scholar] [CrossRef]
- Hagan, T.; Cortese, M.; Rouphael, N.; Boudreau, C.; Linde, C.; Maddur, M.S.; Das, J.; Wang, H.; Guthmiller, J.; Zheng, N.-Y. Antibiotics-driven gut microbiome perturbation alters immunity to vaccines in humans. Cell 2019, 178, 1313–1328.e1313. [Google Scholar] [CrossRef]
- Pichichero, M.E. Variability of vaccine responsiveness in early life. Cell. Immunol. 2023, 393, 104777. [Google Scholar] [CrossRef]
- Siegrist, C.-A. Neonatal and early life vaccinology. Vaccine 2001, 19, 3331–3346. [Google Scholar] [CrossRef]
- Diks, A.M.; Overduin, L.A.; Van Leenen, L.D.; Slobbe, L.; Jolink, H.; Visser, L.G.; Van Dongen, J.J.; Berkowska, M.A. B-cell immunophenotyping to predict vaccination outcome in the immunocompromised-A systematic review. Front. Immunol. 2021, 12, 690328. [Google Scholar] [CrossRef]
- Van Landingham, C.B.; Keast, D.R.; Longnecker, M.P. Serum concentration of antibodies to mumps, but not measles, Rubella, or Varicella, is associated with intake of dietary fiber in the NHANES, 1999–2004. Nutrients 2021, 13, 813. [Google Scholar] [CrossRef]
- Van Hoffen, E.; Ruiter, B.; Faber, J.; M’Rabet, L.; Knol, E.F.; Stahl, B.; Arslanoglu, S.; Moro, G.; Boehm, G.; Garssen, J. A specific mixture of short-chain galacto-oligosaccharide and long-chain fructo-oligosaccharide induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy 2009, 64, 484–487. [Google Scholar] [CrossRef]
- Dinleyici, M.; Barbieur, J.; Dinleyici, E.C.; Vandenplas, Y. Functional effects of human milk oligosaccharide (HMOs). Gut Microbes 2023, 15, 2186115. [Google Scholar] [CrossRef]
- Kassai, S.; de Vos, P. Gastrointestinal barrier function, immunity, and neurocognition: The role of human milk oligosaccharide (hMO) supplementation in infant formula. Compr. Rev. Food Sci. Food Saf. 2024, 23, e13271. [Google Scholar] [CrossRef]
- Xiao, L.; Engen, P.A.; Leusink-Muis, T.; Van Ark, I.; Stahl, B.; Overbeek, S.A.; Garssen, J.; Naqib, A.; Green, S.J.; Keshavarzian, A. The combination of 2′-fucosyllactose with short-chain galacto-oligosaccharide and long-chain fructo-oligosaccharide that enhance influenza vaccine responses is associated with mucosal immune regulation in mice. J. Nutr. 2019, 149, 856–869. [Google Scholar] [CrossRef]
- Tanaka, T.; Narazaki, M.; Kishimoto, T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb. Perspect. Biol. 2014, 6, a016295. [Google Scholar] [CrossRef]
- Liu, Y.; Zhu, Y.; Wang, H.; Wan, L.; Zhang, W.; Mu, W. Strategies for enhancing microbial production of 2′-fucosyllactose, the most abundant human milk oligosaccharide. J. Agric. Food Chem. 2022, 70, 11481–11499. [Google Scholar] [CrossRef]
- Zuurveld, M.; Ayechu-Muruzabal, V.; Folkerts, G.; Garssen, J.; van ‘t Land, B.; Willemsen, L.E. Specific Human milk oligosaccharide Differentially Promote Th1 and Regulatory Responses in a CpG-Activated Epithelial/Immune Cell Coculture. Biomolecules 2023, 13, 263. [Google Scholar] [CrossRef]
- van den Berg, J.P.; Westerbeek, E.A.; van der Klis, F.R.; Berbers, G.A.; Lafeber, H.N.; van Elburg, R.M. Neutral and acidic oligosaccharides supplementation does not increase the vaccine antibody response in preterm infants in a randomized clinical trial. PLoS ONE 2013, 8, e70904. [Google Scholar] [CrossRef]
- Salvini, F.; Riva, E.; Salvatici, E.; Boehm, G.; Jelinek, J.; Banderali, G.; Giovannini, M. A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. J. Nutr. 2011, 141, 1335–1339. [Google Scholar] [CrossRef] [PubMed]
- Black, C.A. Delayed type hypersensitivity: Current theories with a historic perspective. Dermatol. Online J. 1999, 5, 7. [Google Scholar] [CrossRef] [PubMed]
- Schijf, M.A.; Kruijsen, D.; Bastiaans, J.; Coenjaerts, F.E.; Garssen, J.; van Bleek, G.M.; van’t Land, B. Specific dietary oligosaccharides increase Th1 responses in a mouse respiratory syncytial virus infection model. J. Virol. 2012, 86, 11472–11482. [Google Scholar] [CrossRef]
- Chattha, K.S.; Vlasova, A.N.; Kandasamy, S.; Rajashekara, G.; Saif, L.J. Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J. Immunol. 2013, 191, 2446–2456. [Google Scholar] [CrossRef]
- Jacobs, J.P.; Lee, M.L.; Rechtman, D.J.; Sun, A.K.; Autran, C.; Niklas, V. Human milk oligosaccharide modulate the intestinal microbiome of healthy adults. Sci. Rep. 2023, 13, 14308. [Google Scholar] [CrossRef]
- Šuligoj, T.; Vigsnæs, L.K.; Abbeele, P.V.d.; Apostolou, A.; Karalis, K.; Savva, G.M.; McConnell, B.; Juge, N. Effects of human milk oligosaccharide on the adult gut microbiota and barrier function. Nutrients 2020, 12, 2808. [Google Scholar] [CrossRef]
- Walsh, C.; Lane, J.A.; van Sinderen, D.; Hickey, R.M. Human milk oligosaccharide: Shaping the infant gut microbiota and supporting health. J. Funct. Foods 2020, 72, 104074. [Google Scholar] [CrossRef]
- Schönknecht, Y.B.; Moreno Tovar, M.V.; Jensen, S.R.; Parschat, K. Clinical studies on the supplementation of manufactured human milk oligosaccharide: A systematic review. Nutrients 2023, 15, 3622. [Google Scholar] [CrossRef]
- Cho, S.; Samuel, T.M.; Li, T.; Howell, B.R.; Baluyot, K.; Hazlett, H.C.; Elison, J.T.; Zhu, H.; Hauser, J.; Sprenger, N.; et al. Interactions between Bifidobacterium and Bacteroides and human milk oligosaccharide and their associations with infant cognition. Front. Nutr. 2023, 10, 1216327. [Google Scholar] [CrossRef]
- Zhang, B.; Li, L.-Q.; Liu, F.; Wu, J.-Y. Human milk oligosaccharide and infant gut microbiota: Molecular structures, utilization strategies and immune function. Carbohydr. Polym. 2022, 276, 118738. [Google Scholar] [CrossRef]
- Wan, J.; An, L.; Ren, Z.; Wang, S.; Yang, H.; Ma, J. Effects of galactooligosaccharides on maternal gut microbiota, glucose metabolism, lipid metabolism and inflammation in pregnancy: A randomized controlled pilot study. Front. Endocrinol. 2023, 14, 1034266. [Google Scholar] [CrossRef] [PubMed]
- Cheon, S.; Kim, G.; Bae, J.-H.; Lee, D.H.; Seong, H.; Kim, D.H.; Han, J.-S.; Lim, S.-Y.; Han, N.S. Comparative analysis of prebiotic effects of four oligosaccharides using in vitro gut model: Digestibility, microbiome, and metabolome changes. FEMS Microbiol. Ecol. 2023, 99, fiad002. [Google Scholar] [CrossRef] [PubMed]
- Mahalak, K.K.; Firrman, J.; Narrowe, A.B.; Hu, W.; Jones, S.M.; Bittinger, K.; Moustafa, A.M.; Liu, L. Fructooligosaccharides (FOS) differentially modifies the in vitro gut microbiota in an age-dependent manner. Front. Nutr. 2023, 9, 1058910. [Google Scholar] [CrossRef]
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Azarmi, M.; Seyed Toutounchi, N.; Hogenkamp, A.; Thijssen, S.; Overbeek, S.A.; Garssen, J.; Folkerts, G.; van’t Land, B.; Braber, S. Human Milk Oligosaccharides in Combination with Galacto- and Long-Chain Fructo-Oligosaccharides Enhance Vaccination Efficacy in a Murine Influenza Vaccination Model. Nutrients 2024, 16, 2858. https://doi.org/10.3390/nu16172858
Azarmi M, Seyed Toutounchi N, Hogenkamp A, Thijssen S, Overbeek SA, Garssen J, Folkerts G, van’t Land B, Braber S. Human Milk Oligosaccharides in Combination with Galacto- and Long-Chain Fructo-Oligosaccharides Enhance Vaccination Efficacy in a Murine Influenza Vaccination Model. Nutrients. 2024; 16(17):2858. https://doi.org/10.3390/nu16172858
Chicago/Turabian StyleAzarmi, Mehrdad, Negisa Seyed Toutounchi, Astrid Hogenkamp, Suzan Thijssen, Saskia A. Overbeek, Johan Garssen, Gert Folkerts, Belinda van’t Land, and Saskia Braber. 2024. "Human Milk Oligosaccharides in Combination with Galacto- and Long-Chain Fructo-Oligosaccharides Enhance Vaccination Efficacy in a Murine Influenza Vaccination Model" Nutrients 16, no. 17: 2858. https://doi.org/10.3390/nu16172858