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Joann Kerperien IMMUNOMODULATORY PROPERTIES OF DIETARY NON-DIGESTIBLE GALACTO-, FRUCTO- AND ACIDIC-OLIGOSACCHARIDES IN VACCINATION AND COW’S MILK ALLERGY JOANN KERPERIEN JOANN MILK ALLERGY AND COW’S IN VACCINATION AND ACIDIC-OLIGOSACCHARIDES FRUCTO- NON-DIGESTIBLE GALACTO-, PROPERTIES OF DIETARY IMMUNOMODULATORY Mucosal and systemic immune-regulation by fermentable fi bers IMMUNOMODULATORY PROPERTIES OF DIETARY NON-DIGESTIBLE GALACTO-, FRUCTO- AND ACIDIC- OLIGOSACCHARIDES IN VACCINATION AND COW’S MILK ALLERGY Mucosal and systemic immunoregulation by fermentable fi bers JoAnn Kerperien IMMUNOMODULATORY PROPERTIES OF DIETARY NON-DIGESTIBLE GALACTO-, FRUCTO- AND ACIDIC-OLIGOSACCHARIDES IN VACCINATION AND COW’S MILK ALLERGY Mucosal and systemic immunoregulation by oligosaccharides JoAnn Kerperien 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 1 ISBN: 978-90-393-7137-4 Thesis and Cover Design: Studio 0404, Nijmegen Printed by: Ipskamp Printing, Enschede, The Netherlands © JoAnn Kerperien, 2019, Nijmegen, The Netherlands All rights reserved. No part of this thesis publication may be reproduced, stored in a retrieval system of any nature, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, included a complete or partial transcription, without the prior written permission of the author. Application for this should be addressed to the author. The research conducted in this thesis was financially supported by the Utrecht Institute for Pharmaceutical Sciences and Nutricia Research B.V. 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 2 IMMUNOMODULATORY PROPERTIES OF DIETARY NON-DIGESTIBLE GALACTO-, FRUCTO- AND ACIDIC-OLIGOSACCHARIDES IN VACCINATION AND COW’S MILK ALLERGY Mucosal and systemic immunoregulation by oligosaccharides Immunomodulatoire eigenschappen door dieetinterventie met onverteerbare galacto-, fructo- en zure- oligosachariden tijdens vaccinatie en bij koemelkallergie Systemische en mucosale immunoregulatie door oligosachariden (met een samenvatting in het Nederlands) PROEFSCHRIFT Ter verkrijging van de graad van doctor aan de Universiteit Utrecht op gezag van de rector magnificus, prof. Dr. H.R.B.M. Kummeling ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op maandag 17 juni 2019 des middags te 2.30 uur door JoAnn Kerperien Geboren op 23 juni 1980 te Borculo 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 3 Promotor: Prof. Dr. J. Garssen Copromotor: Dr. L.E.M. Willemsen Dr. L.M.J. Knippels The publication of this thesis was financially supported by: Nutricia Research, B.V. 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 4 …. I can go the distance, and I’ll stay on track, no I won’t accept defeat, It’s an uphill slope, but I won’t lose hope, ‘till I go the distance….. Go the distance, Hercules 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 5 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 6 ‘Voor de wereld was jij maar iemand, voor mij was jij de wereld’ Mijn laatste belofte aan jou heb ik hiermee volbracht. Voor mijn allerliefste mama Anke Kerperien 1960- 2015 † 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 7 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 8 TABLE OF CONTENTS Chapter 1 General introduction 11 Chapter 2 De velopment of the immune system; Early nutrition and 21 consequences for later life Chapter 3 Non-diges tible oligosaccharides modulate intestinal 49 immune activation and suppress cow’s milk allergic symptoms Chapter 4 IL10r or TGFβ neutralization abrogates the protective effect 67 of a specific non-digestible oligosaccharide mixture in cow’s milk allergic mice Chapter 5 Alt erations in regulatory T cells induced by specific 89 oligosaccharides improve vaccine responsiveness in mice Chapter 6 Diet ary vitamin D supplementation is ineffective in 107 preventing murine cow’s milk allergy, irrespective of the presence of non-digestible oligosaccharides Chapter 7 Diet ary vitamin A supports a mixture of specific non- 133 digestible oligosaccharides in the prevention of cow’s milk allergic symptoms in mice Chapter 8 General discussion 163 Abbreviations 181 Appendix Nederlandse samenvatting 189 Dankwoord 197 Curriculum Vitae 203 Publications 205 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 9 1 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 10 General 1 introduction 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 11 CHAPTER 1 12 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 12 GENERAL INTRODUCTION GENERAL INTRODUCTION 1 The prevalence of allergic diseases has been rising in industrialized countries over the last decades (1). Often the first allergy to develop in early life is a food allergy. The risk of developing food allergy is increasing in the developed world and it has been suggested that food allergy is a disease of the more educated upper class (1). Furthermore, more children with food allergies are found in cities than in rural areas (1). Also there is a possible link between food allergy and the diminishing period of breast feeding, increased consumption of fat and n-6 over n-3 polyunsaturated fatty acids, low vitamin D levels and late introduction of allergenic foods (1). There are several well-known food allergies, such as allergy for egg, cow’s milk, peanut and also for wheat, fish, soy and several other food proteins. Cow’s milk allergy (CMA) is one of the first allergies to develop in life. One to three percent of children develop CMA and symptoms range from behavioral changes, to cutaneous, respiratory, conjunctival, gastrointestinal and cardiovascular reactions ranging from mild symptoms to anaphylaxis, from acute to delayed to chronic (2-4). This allergy which is characterized by acute allergic reactions upon oral ingestion of the culprit food can be IgE mediated or non-IgE mediated (4, 5). Severe allergic reaction to milk and high levels of milk specific IgE can predispose to persistence of the allergy (6, 7). For some allergies, like cow’s milk, egg, wheat or soy, most children will outgrow their allergy (3, 4, 6) although there are studies showing that CMA is getting more persistent (8, 9). Food allergy is not only a personal and social burden, it is also an economic burden (3). Over the recent years more hospitalizations to anaphylaxis from food allergies have been registered (3). Even those who outgrow their food allergy may be more predisposed to develop other allergies later in life. Although there is discussion for more specificity for the term atopic march, food allergy to peanut, egg and milk were significantly associated with the development of asthma and rhinitis (10, 11). So, it is important to find more preventive or treatment possibilities to stop this atopic expansion especially since currently no treatment for food allergy is available. The maternal diet during pregnancy may influence the allergy status in the unborn children which may be maintained throughout life (12). Previously it was advised after birth that children at risk should avoid specific food particles, however this approach is being challenged. Recent studies show that early introduction rather than total avoidance of specific food proteins in the first year of life may be required to prevent development of food allergy (3). This was specifically shown for peanut allergy in the Learning Early About Peanut allergy (LEAP) study (13). In this study it was shown that children with severe eczema, egg allergy or both developed less peanut allergy when consuming products containing peanut (13). This was independent of the susceptibility to develop this allergy at the start of the study (13). Ingestion of baked milk products by children affected with CMA may accelerate and improve oral tolerance induction to milk (6). For now however the only safe option for CMA is total avoidance of the causative food proteins (3, 4, 14). Long lasting permanent tolerance induction via allergen specific 13 530928-L-bw-Kerperien Processed on: 7-5-2019 PDF page: 13 CHAPTER 1 immunotherapy is still a challenge and care should be taken since unwanted allergic side effects often occur. Hence, prevention of food allergy development is an important topic of investigation and dietary intervention with non-digestible oligosaccharides (NDO) alone or in combination with vitamin D and vitamin A may contribute to acquire natural oral tolerance to food proteins directly after birth and in the first year of life (12). Oral tolerance is acquired in the gastro-intestinal tract through a state of non-responsiveness of the immune system to harmless food particles. An allergic reaction is triggered when the immune system incorrectly identifies a food particle as harmful. Knowledge about (oral) tolerance in general comes from murine experimental models (15). Specialized epithelial cells, for example microfold (M) cells, are responsible for capturing antigens from the intestine and shuttling them to the underlying dendritic cells (DC) in the Peyer’s Patches (PP). In the intestine DC and fractalkine (CX3CR1) positive macrophages, sample antigens through the intestinal epithelial layer with cell protrusions, or they acquire particles via the epithelial layer through cell-cell contact and transfer these to immature DC (16). DC present the antigen to cells in the Lamina Propria (LP) or they can travel to the mesenteric lymph nodes (MLN) (15, 17). Both transforming growth factor beta (TGFβ) and interleukin (IL)10 are produced by DC and together with retinoic acid (RA) are held responsible for the development and maintenance of a tolerogenic environment in the MLN and LP of the small intestine (15, 16, 18-21). In this environment regulatory T cell (Treg) subsets are produced in the MLN and the activated Treg, expressing the necessary chemokine receptor CCR9 and integrin α4β7, migrate to the intestinal LP (16). Treg manage different cell populations by cell-cell contact through cytotoxic T-lymphocyte associated protein 4 (CTLA4), lymphocyte activation gene 3 (LAG3) or programmed cell death protein 1 (PD1) and by cytokine production of TGFβ, IL10 and IL35.
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