Pro-inflammatory immunological effects of adipose tissue and risk of food allergy in obesity: Focus on immunological mechanisms
Main Article Content
Keywords
Obesity, Pro-inflammatory, Immunological effects, Adipose tissue, Food allergy
Abstract
Over the past three decades, the number of obese people has risen steadily. The chronic low-grade inflammatory state and the non-specific activation of the immune system have contributed greatly to the development of obesity-related immunology. Food allergy as a kind of inflammatory disease with abnormal immune response may be associated with obesity. This review begins with the pro-inflammatory immunological effects of adipose tissue in obesity, and explains the possible effects of obesity on food allergy. In short, obesity not only directly causes imbalance of allergic-related immune cells in adipose tissue, but also indirectly causes this consequence through affecting expression of adipocytokines and peroxisome proliferator-activated receptor gamma (PPAR) in adipose tissue. As a result, circulating levels of pro-inflammatory factors which are partly derived from adipose tissue increase, which might cause intestinal barrier injury. Therefore, obesity may increase the risk of food allergy.
References
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36. Huang W, Glass CK. Nuclear receptors and inflammation control: molecular mechanisms and pathophysiological relevance. Arterioscler Thromb Vasc Biol. 2010;30(8):1542-9.
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38. Shamsi BH, Ma C, Naqvi S, Xiao Y. Effects of pioglitazone mediated activation of PPAR- on CIDEC and obesity related changes in mice. PLoS One. 2014;9(9):e106992.
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49. Smale ST. Hierarchies of NF-B target-gene regulation. Nat Immunol. 2011;12(8):689---94.
50. Supajatura V, Ushio H, Nakao A, Akira S, Okumura K, Ra C, et al. Differential responses of mast cell toll-like receptors 2 and 4 in allergy and innate immunity. J Clin Invest. 2002;109(10):1351---9.
51. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 2010;72(1):219---46.
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54. Zhang Y, Li X, Fang S, Zhu Z, Yao M, Ying L, et al. Peroxisome proliferator-activated receptor agonist suppresses mast cell maturation and induces apoptosis. Mol Med Rep. 2017;16(2):1793---800.
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56. Hussain M, Bonilla-Rosso G, Kwong Chung CKC, Bariswyl L, Rodriguez MS, Kim BS, et al. High dietary fat intake induces a microbiota signature that promotes food allergy. J Allergy Clin Immunol. 2019;144:157---70, http://dx.doi.org/10.1016/j.jaci.2019.01.043.
2. Sideleva O, Suratt BT, Black KE, Tharp WG, Pratley RE, Forgione P, et al. Obesity and asthma: an inflammatory disease of adipose tissue not the airway. Am J Respir Crit Care. 2012;186(7):598-605.
3. Luo X, Xiang J, Dong X, Cai F, Suo J, Wang Z, Liu M. Association between obesity and atopic disorders in Chinese adults: an individually matched case-control study. BMC Public Health. 2013;13(1):12.
4. D’Auria E, Abrahams M, Zuccotti GV, Venter C. Personalized nutrition approach in food allergy: is it prime time yet? Nutrients. 2019;11(2):359.
5. Sicherer SH, Sampson HA. Food allergy: epidemiology, pathogenesis, diagnosis, and treatment. J Allergy Clin Immun. 2014;133(2):291-307.
6. Balistreri CR, Caruso C, Candore G. The role of adipose tissue and adipokines in obesity-related inflammatory diseases. Mediat Inflamm. 2010;2010:1-19.
7. Ozmen F, Ozmen MM. Obesity, immunology and obesity surgery. Adv Obes Weight Manag Control. 2016;4:27-30.
8. Han JM, Levings MK. Immune regulation in obesity-associated adipose inflammation. J Immunol. 2013;191(2):527532.
9. Szanto A, Nagy L. The many faces of PPAR: anti-inflammatory by any means? Immunobiology. 2008;213(9-10):789803.
10. Garcia-Fuentes E, Murri M, Garrido-Sanchez L, Garcia-Serrano S, García-Almeida JM, Moreno-Santos I, et al. PPAR expression after a high-fat meal is associated with plasma superoxide dismutase activity in morbidly obese persons. Obesity. 2010;18(5):952-8.
11. Apostolopoulos V, de Courten MP, Stojanovska L, Blatch GL, Tangalakis K, de Courten B. The complex immunological and inflammatory network of adipose tissue in obesity. Mol Nutr Food Res. 2016;60(1):43-57.
12. Visness CM, London SJ, Daniels JL, Kaufman JS, Yeatts KB, SiegaRiz AM, et al. Association of obesity with IgE levels and allergy symptoms in children and adolescents: results from the National Health and Nutrition Examination Survey 2005-2006. J Allergy Clin Immun. 2009;123(5):1163-9.
13. Leung TF, Kong AP, Chan IH, Choi KC, Ho CS, Chan MH, et al. Association between obesity and atopy in Chinese schoolchildren. Int Arch Allergy Immunol. 2009;149(2):133-40.
14. Bruno A, Pace E, Cibella F, Chanez P. Body mass index and comorbidities in adult severe asthmatics. Biomed Res Int. 2014;2014:1-7.
15. Schipper HS, Prakken B, Kalkhoven E, Boes M. Adipose tissue-resident immune cells: key players in immunometabolism. Trends Endocrinol Metab. 2012;23(8):407-15.
16. Schipper HS, Rakhshandehroo M, van de Graaf SF, Venken K, Koppen A, Stienstra R, et al. Natural killer T cells in adipose tissue prevent insulin resistance. J Clin Invest. 2012;122(9): 3343-54.
17. Baltimore D. NF-B is 25. Nat Immunol. 2011;12(8):683.
18. Brigeliusflohé R, Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal. 2011;15(8):2335-81.
19. Cui W, Li LX, Sun CM, Wen Y, Zhou Y, Dong YL, et al. Tumor necrosis factor alpha increases epithelial barrier permeability by disrupting tight junctions in Caco-2 cells. Braz J Med Biol Res. 2010;43(4):330-7.
20. Leiria LO, Martins MA, Saad MJA. Obesity and asthma: beyond TH2 inflammation. Metabolism. 2015;64(2):172-81.
21. Sogut A, Yilmaz O, Kirmaz C, Ozbilgin K, Onur E, Celik O, et al. Regulatory-T, T-helper 1, and T-helper 2 cell differentiation in nasal mucosa of allergic rhinitis with olive pollen sensitivity. Int Arch Allergy Immunol. 2011;157(4):349353.
22. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med. 2009;15(8):930-9.
23. Jeffrey D, Zubair S, Nilay S, Needleman B, Mikami D, Narula V, et al. Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PLoS One. 2011;6(1):e16376.
24. Wagner NM, Brandhorst G, Czepluch F, Lankeit M, Eberle C, Herzberg S, et al. Circulating regulatory T cells are reduced in obesity and may identify subjects at increased metabolic and cardiovascular risk. Obesity. 2013;21(3): 461-8.
25. Sly LM, Kalesnikoff J, Lam V, Wong D, Song C, Omeis S, et al. IgE-induced mast cell survival requires the prolonged generation of reactive oxygen species. J Immunol. 2008;181(6): 3850-60.
26. Poglio S, Toni-Costes FD, Arnaud E, Laharrague P, Espinosa E, Casteilla L, et al. Adipose tissue as a dedicated reservoir of functional mast cell progenitors. Stem Cells. 2010;28(11):2065-72.
27. Altintas MM, Rossetti MA, Nayer B, Puig A, Zagallo P, Ortega LM, et al. Apoptosis, mastocytosis, and diminished adipocytokine gene expression accompany reduced epididymal fat mass in long-standing diet-induced obese mice. Lipids Health Dis. 2011;10(1):198.
28. Liu J, Adeline D, Sun J, Zhang J, Clément K, Glickman JN, et al. Deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med. 2009;15(8):940-5.
29. Jacob C, Yang PC, Darmoul D, Amadesi S, Saito T, Cottrell GS, et al. Mast cell tryptase controls paracellular permeability of the intestine: role of protease-activated receptor 2 and -arrestins. J Biol Chem. 2005;280(36):3193631948.
30. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol. 2011;11(2):85-97.
31. Naylor C, Jr PW. Leptin regulation of immune responses. Trends Mol Med. 2016;22:88-98.
32. Ohashi K, Yuasa D, Shibata R, Murohara T, Ouchi N. Adiponectin as a target in obesity-related inflammatory state. Endocr Metab Immune. 2015;15(2):145-50.
33. Hersoug LG, Linneberg A. The link between the epidemics of obesity and allergic diseases: does obesity induce decreased immune tolerance? Allergy. 2007;62(10):1205-13.
34. Gupta RA, Polk DB, Krishna U, Israel DA, Yan F, DuBois RN. Activation of peroxisome proliferator-activated receptor gamma suppresses nuclear factor kappa B-mediated apoptosis induced by Helicobacter pylori in gastric epithelial cells. J Biol Chem. 2001;276(33):31059-66.
35. Kersten S, Desvergne B, Wahli W. Roles of PPARs in health and disease. Nature. 2000;405(6785):421-4.
36. Huang W, Glass CK. Nuclear receptors and inflammation control: molecular mechanisms and pathophysiological relevance. Arterioscler Thromb Vasc Biol. 2010;30(8):1542-9.
37. Lehrke M, Lazar MA. The many faces of PPAR. Cell. 2005;123(6):993-9.
38. Shamsi BH, Ma C, Naqvi S, Xiao Y. Effects of pioglitazone mediated activation of PPAR- on CIDEC and obesity related changes in mice. PLoS One. 2014;9(9):e106992.
39. Gayet C, Leray V, Saito M, Siliart B, Nguyen P. The effects of obesity-associated insulin resistance on mRNA expression of peroxisome proliferator-activated receptor-gamma target genes, in dogs. Br J Nutr. 2007;98(3):497-503.
40. Choi JH, Banks AS, Estall JL, Kajimura Shingo, Bostrom Pontus, Laznik Dina, et al. Obesity-linked phosphorylation of PPAR by cdk5 is a direct target of the anti-diabetic PPAR ligands. Nature. 2010;466(7305):451-6.
41. Banks AS, Mcallister FE, Camporez JPG, Zushin PJ, Jurczak MJ, Laznik-Bogoslavski D, et al. An ERK/Cdk5 axis controls the diabetogenic actions of PPAR. Nature. 2014;517(7534):391-5.
42. Motawi TK, Shaker OG, Ismail MF, Sayed NH. Peroxisome proliferator-activated receptor-gamma in obesity and colorectal cancer: the role of epigenetics. Sci Rep-UK. 2017;7(1):10714.
43. Yuan G, Chen X, Li D. Modulation of peroxisome proliferator-activated receptor gamma (PPAR ) by conjugated fatty acid in obesity and inflammatory bowel disease. J Agric Food Chem. 2015;63(7):1883-95.
44. Zhou XR, Sun CH, Liu JR, Zhao D. Dietary conjugated linoleic acid increases PPAR gene expression in adipose tissue of obese rat, and improves insulin resistance. Growth Horm IGF Res. 2008;18(5):361-8.
45. Rao YPC, Lokesh BR. Down-regulation of NF-B expression by n-3 fatty acid-rich linseed oil is modulated by PPAR activation, eicosanoid cascade and secretion of cytokines by macrophages in rats fed partially hydrogenated vegetable fat. Eur J Nutr. 2017;56(3):1135-47.
46. Neschen S, Morino K, Rossbacher JC, Pongratz RL, Cline GW, Sono S, et al. Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-gamma-dependent mechanism in mice. Diabetes. 2006;55(4):924-8.
47. Welch JS, Ricote M, Akiyama TE, Gonzalez FJ, Glass CK. PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc Natl Acad Sci USA. 2003;100(11):67126717.
48. Morales JK, Falanga YT, Depcrynski A, Fernando J, Ryan JJ. Mast cell homeostasis and the JAK---STAT pathway. Genes Immun. 2010;11(8):599---608.
49. Smale ST. Hierarchies of NF-B target-gene regulation. Nat Immunol. 2011;12(8):689---94.
50. Supajatura V, Ushio H, Nakao A, Akira S, Okumura K, Ra C, et al. Differential responses of mast cell toll-like receptors 2 and 4 in allergy and innate immunity. J Clin Invest. 2002;109(10):1351---9.
51. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 2010;72(1):219---46.
52. Cipolletta D, Feuerer M, Li A, Kamei N, Lee J, Shoelson SE, et al. PPAR- is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature. 2012;486(7404):549---53.
53. Sugiyama H, Nonaka T, Kishimoto T, Komoriya K, Tsuji K, Nakahata T. Peroxisome proliferator-activated receptors are expressed in mouse bone marrow-derived mast cells. Febs Lett. 2000;467(2):259---62.
54. Zhang Y, Li X, Fang S, Zhu Z, Yao M, Ying L, et al. Peroxisome proliferator-activated receptor agonist suppresses mast cell maturation and induces apoptosis. Mol Med Rep. 2017;16(2):1793---800.
55. Tachibana M, Wada K, Katayama K, Kamisaki Y, Maeyama K, Kadowaki T, et al. Activation of peroxisome proliferator-activated receptor-gamma suppresses mast cell maturation involved in allergic diseases. Allergy. 2010;63(9):1136---47.
56. Hussain M, Bonilla-Rosso G, Kwong Chung CKC, Bariswyl L, Rodriguez MS, Kim BS, et al. High dietary fat intake induces a microbiota signature that promotes food allergy. J Allergy Clin Immunol. 2019;144:157---70, http://dx.doi.org/10.1016/j.jaci.2019.01.043.
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May 15, 2020
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Guo, X., Cheng, L., Yang, S., & Che, H. (2020). Pro-inflammatory immunological effects of adipose tissue and risk of food allergy in obesity: Focus on immunological mechanisms. Allergologia Et Immunopathologia, 48(3), 306-312. https://all-imm.com/index.php/aei/article/view/214
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How to Cite
Guo, X., Cheng, L., Yang, S., & Che, H. (2020). Pro-inflammatory immunological effects of adipose tissue and risk of food allergy in obesity: Focus on immunological mechanisms. Allergologia Et Immunopathologia, 48(3), 306-312. https://all-imm.com/index.php/aei/article/view/214