Research article Topical Sections

Allergic sensitization to peanuts is enhanced in mice fed a high-fat diet

  • Received: 14 August 2020 Accepted: 08 October 2020 Published: 10 October 2020
  • The incidence of peanut (PN) allergy is on the rise. As peanut allergy rates have continued to climb over the past few decades, obesity rates have increased to record highs, suggesting a link between obesity and the development of peanut allergy. While progress has been made, much remains to be learned about the mechanisms driving the development of allergic immune responses to peanut. Remaining unclear is whether consuming a Western diet, a diet characterized by overeating foods rich in saturated fat, salt, and refined sugars, supports the development of PN allergy. To address this, we fed mice a high fat diet to induce obesity. Once diet-induced obesity was established, mice were exposed to PN flour via the airways using our 4-week inhalation model. Mice were subsequently challenged with PN extract to induce anaphylaxis. Mice fed a high-fat diet developed significantly higher titers of PN-specific IgE, as well as stronger anaphylactic responses, when compared to their low-fat diet fed counterparts. These results suggest that obesity linked to eating a high-fat diet promotes the development of allergic immune responses to PN in mice. Such knowledge is critical to advance our growing understanding of the immunology of PN allergy.

    Citation: Joseph J. Dolence, Hirohito Kita. Allergic sensitization to peanuts is enhanced in mice fed a high-fat diet[J]. AIMS Allergy and Immunology, 2020, 4(4): 88-99. doi: 10.3934/Allergy.2020008

    Related Papers:

  • The incidence of peanut (PN) allergy is on the rise. As peanut allergy rates have continued to climb over the past few decades, obesity rates have increased to record highs, suggesting a link between obesity and the development of peanut allergy. While progress has been made, much remains to be learned about the mechanisms driving the development of allergic immune responses to peanut. Remaining unclear is whether consuming a Western diet, a diet characterized by overeating foods rich in saturated fat, salt, and refined sugars, supports the development of PN allergy. To address this, we fed mice a high fat diet to induce obesity. Once diet-induced obesity was established, mice were exposed to PN flour via the airways using our 4-week inhalation model. Mice were subsequently challenged with PN extract to induce anaphylaxis. Mice fed a high-fat diet developed significantly higher titers of PN-specific IgE, as well as stronger anaphylactic responses, when compared to their low-fat diet fed counterparts. These results suggest that obesity linked to eating a high-fat diet promotes the development of allergic immune responses to PN in mice. Such knowledge is critical to advance our growing understanding of the immunology of PN allergy.


    加载中

    Acknowledgments



    This work was supported by grants from the National Institutes of Health (NIH): R01 AI71106 to Hirohito Kita and Joseph Dolence was supported by a T32 Training Grant in Allergic Diseases. Additional funding was provided by the Mayo Foundation. Joseph Dolence is supported by grants from the National Center for Research Resources (NCRR; 5P20RR016469) and the National Institute for General Medical Science (NIGMS; 8P20GM103427), a component of the NIH. We would also like to thank Dr. Koji Iijima for bleeding mice, and Dr. Kimberly Carlson for editing the manuscript.

    Conflict of interests



    All authors declare no conflicts of interest in this paper.

    [1] Hales CM, Fryar CD, Carroll MD, et al. (2018) Trends in obesity and severe obesity prevalence in US youth and adults by sex and age, 2007–2008 to 2015–2016. Jama 319: 1723-1725. doi: 10.1001/jama.2018.3060
    [2] Togias A, Cooper SF, Acebal ML, et al. (2017) Addendum guidelines for the prevention of peanut allergy in the United States: Report of the National Institute of Allergy and Infectious Diseases-sponsored expert panel. J Allergy Clin Immunol 139: 29-44. doi: 10.1016/j.jaci.2016.10.010
    [3] Thorburn AN, Macia L, Mackay CR (2014) Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity 40: 833-842. doi: 10.1016/j.immuni.2014.05.014
    [4] Myles IA (2014) Fast food fever: reviewing the impacts of the Western diet on immunity. Nutr J 13: 61. doi: 10.1186/1475-2891-13-61
    [5] Hussain M, Bonilla-Rosso G, Kwong CKCK, et al. (2019) High dietary fat intake induces a microbiota signature that promotes food allergy. J Allergy Clin Immunol 144: 157-170. doi: 10.1016/j.jaci.2019.01.043
    [6] Ley RE, Backhed F, Turnbaugh P, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102: 11070-11075. doi: 10.1073/pnas.0504978102
    [7] Turnbaugh PJ, Backhed F, Fulton L, et al. (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213-223. doi: 10.1016/j.chom.2008.02.015
    [8] Huang EY, Leone VA, Devkota S, et al. (2013) Composition of dietary fat source shapes gut microbiota architecture and alters host inflammatory mediators in mouse adipose tissue. JPEN J Parenter Enteral Nutr 37: 746-754. doi: 10.1177/0148607113486931
    [9] David LA, Maurice CF, Carmody RN, et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563. doi: 10.1038/nature12820
    [10] Carmody RN, Gerber GK, Luevano JM, et al. (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17: 72-84. doi: 10.1016/j.chom.2014.11.010
    [11] Lam YY, Ha CW, Campbell CR, et al. (2012) Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS One 7: e34233. doi: 10.1371/journal.pone.0034233
    [12] Wesemann DR, Nagler CR (2016) The microbiome, timing, and barrier function in the context of allergic disease. Immunity 44: 728-738. doi: 10.1016/j.immuni.2016.02.002
    [13] Volynets V, Louis S, Pretz D, et al. (2017) Intestinal barrier function and the gut microbiome are differentially affected in mice fed a western-style diet or drinking water supplemented with fructose. J Nutr 147: 770-780. doi: 10.3945/jn.116.242859
    [14] Arias-Jayo N, Abecia L, Alonso-Saez L, et al. (2018) High-fat diet consumption induces microbiota dysbiosis and intestinal inflammation in zebrafish. Microb Ecol 76: 1089-1101. doi: 10.1007/s00248-018-1198-9
    [15] Noval Rivas M, Burton OT, Wise P, et al. (2013) A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol 131: 201-212. doi: 10.1016/j.jaci.2012.10.026
    [16] Stefka AT, Feehley T, Tripathi P, et al. (2014) Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A 111: 13145-13150. doi: 10.1073/pnas.1412008111
    [17] Dolence JJ, Kobayashi T, Iijima K, et al. (2018) Airway exposure initiates peanut allergy by involving the IL-1 pathway and T follicular helper cells in mice. J Allergy Clin Immunol 142: 1144-1158. doi: 10.1016/j.jaci.2017.11.020
    [18] Smarr CB, Hsu CL, Byrne AJ, et al. (2011) Antigen-fixed leukocytes tolerize Th2 responses in mouse models of allergy. J Immunol 187: 5090-5098. doi: 10.4049/jimmunol.1100608
    [19] Wang CY, Liao JK (2012) A mouse model of diet-induced obesity and insulin resistance. Methods Mol Biol 821: 421-433. doi: 10.1007/978-1-61779-430-8_27
    [20] Inui A (2003) Obesity—a chronic health problem in cloned mice? Trends Pharmacol Sci 24: 77-80. doi: 10.1016/S0165-6147(02)00051-2
    [21] Frederich RC, Hamann A, Anderson S, et al. (1995) Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med 1: 1311-1314. doi: 10.1038/nm1295-1311
    [22] Lin S, Thomas TC, Storlien LH, et al. (2000) Development of high fat diet-induced obesity and leptin resistance in C57Bl/6J mice. Int J Obes 24: 639-646. doi: 10.1038/sj.ijo.0801209
    [23] Van Heek M, Compton DS, France CF, et al. (1997) Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J Clin Invest 99: 385-390. doi: 10.1172/JCI119171
    [24] Weisberg SP, McCann D, Desai M, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808. doi: 10.1172/JCI200319246
    [25] Xu H, Barnes GT, Yang Q, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830. doi: 10.1172/JCI200319451
    [26] Silva F, Oliveira EE, Ambrosio MGE, et al. (2020) High-fat diet-induced obesity worsens TH2 immune response and immunopathologic characteristics in murine model of eosinophilic oesophagitis. Clin Exp Allergy 50: 244-255. doi: 10.1111/cea.13533
    [27] Anhe GF, Page CP, et al. (2020) Sex differences in the influence of obesity on a murine model of allergic lung inflammation. Clin Exp Allergy 50: 256-266. doi: 10.1111/cea.13541
    [28] Johnston RA, Zhu M, Rivera-Sanchez YM, et al. (2007) Allergic airway responses in obese mice. Am J Respir Crit Care Med 176: 650-658. doi: 10.1164/rccm.200702-323OC
    [29] Arias K, Chu DK, Flader K, et al. (2011) Distinct immune effector pathways contribute to the full expression of peanut-induced anaphylactic reactions in mice. J Allergy Clin Immunol 127: 1552-1561. doi: 10.1016/j.jaci.2011.03.044
    [30] Krempski JW, Kobayashi T, Iijima K, et al. (2020) Group 2 innate lymphoid cells promote development of T follicular helper cells and initiate allergic sensitization to peanuts. J Immunol 204: 3086-3096. doi: 10.4049/jimmunol.2000029
    [31] Kuroda E, Ozasa K, Temizoz B, et al. (2016) Inhaled fine particles induce alveolar macrophage death and interleukin-1α release to promote inducible bronchus-associated lymphoid tissue formation. Immunity 45: 1299-1310. doi: 10.1016/j.immuni.2016.11.010
    [32] Tashiro H, Takahashi K, Sadamatsu H, et al. (2017) Saturated fatty acid increases lung macrophages and augments house dust mite-induced airway inflammation in mice fed with high-fat diet. Inflammation 40: 1072-1086. doi: 10.1007/s10753-017-0550-4
    [33] Dixon AE, Peters U (2018) The effect of obesity on lung function. Expert Rev Respir Med 12: 755-767. doi: 10.1080/17476348.2018.1506331
    [34] Periyalil HA, Wood LG, Wright TA, et al. (2018) Obese asthmatics are characterized by altered adipose tissue macrophage activation. Clin Exp Allergy 48: 641-649. doi: 10.1111/cea.13109
    [35] Liu J, Divoux A, Sun J, et al. (2009) Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 15: 940-945. doi: 10.1038/nm.1994
    [36] Sicherer SH, Burks AW, Sampson HA (1998) Clinical features of acute allergic reactions to peanut and tree nuts in children. Pediatrics 102: e6. doi: 10.1542/peds.102.1.e6
    [37] Du Toit G, Roberts G, Sayre PH, et al. (2015) Randomized trial of peanut consumption in infants at risk for peanut allergy. N Engl J Med 372: 803-813. doi: 10.1056/NEJMoa1414850
    [38] Trendelenburg V, Ahrens B, Wehrmann AK, et al. (2013) Peanut allergen in house dust of eating area and bed—a risk factor for peanut sensitization? Allergy 68: 1460-1462. doi: 10.1111/all.12226
    [39] Brough HA, Santos AF, Makinson K, et al. (2013) Peanut protein in household dust is related to household peanut consumption and is biologically active. J Allergy Clin Immunol 132: 630-638. doi: 10.1016/j.jaci.2013.02.034
    [40] Smeekens JM, Immormino RM, Balogh PA, et al. (2019) Indoor dust acts as an adjuvant to promote sensitization to peanut through the airway. Clin Exp Allergy 49: 1500-1511. doi: 10.1111/cea.13486
  • Reader Comments
  • © 2020 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(475) PDF downloads(34) Cited by(0)

Article outline

Figures and Tables

Figures(3)  /  Tables(1)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog