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2024 Vol.54, Issue 4 Preview Page

Original Article

Differential Effects of Western and High-fat Diets on the Acceleration of Psoriatic Inflammation
Minji Park1
,
Kyudo Park2
,
YunJae Jung12*
1Department of Health Science and Technology, Gachon Advanced Institute for Health Science & Technology, Gachon University, Incheon 21999, Republic of Korea
2Department of Microbiology, College of Medicine, Lee Gil Ya Cancer and Diabetes Institute, Gachon University, Incheon 21999, Republic of Korea
*yjjung@gachon.ac.kr
31 December 2024. pp. 367-378
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Abstract

Diet-induced metabolic changes can aggravate psoriatic inflammation. This study investigated the distinct inflammatory effects induced by a high-fat diet (HFD) and Western diet (WD) in mice by inducing psoriatic inflammation using topical imiquimod following 12 weeks on either diet. Both diets resulted in increased body weight and perigonadal fat mass compared to a chow diet, with HFD-fed mice gaining more weight. Fasting glucose levels were significantly elevated only in the HFD group. During psoriatic inflammation, WD-fed mice exhibited more pronounced weight loss and aggravated clinical signs of psoriasis. Systemic inflammatory responses, indicated by spleen weight and soluble CD14 serum levels, were increased in both HFD- and WD-fed mice compared to the chow-fed group, with no significant difference between the two diet groups. However, localized inflammatory responses in skin lesions were more pronounced in WD-fed mice, with increased expression of inflammatory mediators. The intestinal immune environment and microbiome composition showed no significant differences between the diet groups. Transcriptomic analysis of skin lesions identified differentially expressed genes, with WD-fed mice enriched in gene sets related to inflammation, keratinization, and cornified envelope formation. In contrast, HFD-fed mice were enriched in genes related to tissue microenvironment remodeling. These findings suggest that WD exacerbates psoriatic skin inflammation more than HFD by promoting inflammatory responses in the skin, highlighting diet-specific impacts on localized inflammation.

Keywords
Psoriasis
Obesity
High-fat diet
Western diet
Diet-induced inflammatory responses
References
1

Christophers E. Psoriasis--epidemiology and clinical spectrum. Clin Exp Dermatol. 2001;26(4):314-320.

10.1046/j.1365-2230.2001.00832.x11422182
2

Griffiths CE, Barker JN. Pathogenesis and clinical features of psoriasis. Lancet. 2007;370(9583):263-271.

10.1016/S0140-6736(07)61128-317658397
3

Balan R, Grigoraş A, Popovici D, Amălinei C. The histopathological landscape of the major psoriasiform dermatoses. Arch Clin Cases. 2021;6(3):59-68.

10.22551/2019.24.0603.1015534754910PMC8565680
4

Kim HJ, Roh JY, Jung Y. Eosinophils accelerate pathogenesis of psoriasis by supporting an inflammatory milieu that promotes neutrophil infiltration. J Invest Dermatol. 2018;138(10):2185-2194.

10.1016/j.jid.2018.03.150929580867
5

Hao Y, Zhu YJ, Zou S, Zhou P, Hu YW, Zhao QX, et al. Metabolic Syndrome and Psoriasis: Mechanisms and Future Directions. Front Immunol. 2021;12:711060.

10.3389/fimmu.2021.71106034367173PMC8343100
6

Griffiths CEM, Armstrong AW, Gudjonsson JE, Barker JNWN. Psoriasis. Lancet. 2021;397(10281):1301-1315.

10.1016/S0140-6736(20)32549-633812489
7

Mathis D. Immunological goings-on in visceral adipose tissue. Cell Metab. 2013;17(6):851-859.

10.1016/j.cmet.2013.05.00823747244PMC4264591
8

Chen YJ, Ho HJ, Tseng CH, Lai ZL, Shieh JJ, Wu CY. Intestinal microbiota profiling and predicted metabolic dysregulation in psoriasis patients. Exp Dermatol. 2018;27(12):1336-1343.

10.1111/exd.1378630238519
9

Yu S, Wu X, Zhou Y, Sheng L, Jena PK, Han D, et al. A Western Diet, but Not a High-Fat and Low-Sugar Diet, Predisposes Mice to Enhanced Susceptibility to Imiquimod-Induced Psoriasiform Dermatitis. J Invest Dermatol. 2019;139(6):1404-1407.

10.1016/j.jid.2018.12.00230571973PMC7574630
10

Nakamizo S, Honda T, Adachi A, Nagatake T, Kunisawa J, Kitoh A, et al. High fat diet exacerbates murine psoriatic dermatitis by increasing the number of IL-17-producing gammadelta T cells. Sci Rep. 2017;7(1):14076.

10.1038/s41598-017-14292-129074858PMC5658347
11

Shi Z, Wu X, Yu S, Huynh M, Jena PK, Nguyen M, et al. Short-Term Exposure to a Western Diet Induces Psoriasiform Dermatitis by Promoting Accumulation of IL-17A-Producing gammadelta T Cells. J Invest Dermatol. 2020;140(9):1815-1823.

10.1016/j.jid.2020.01.02032057839PMC7537492
12

Herbert D, Franz S, Popkova Y, Anderegg U, Schiller J, Schwede K, et al. High-Fat Diet Exacerbates Early Psoriatic Skin Inflammation Independent of Obesity: Saturated Fatty Acids as Key Players. J Invest Dermatol. 2018;138(9):1999-2009.

10.1016/j.jid.2018.03.152229605673
13

Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-15550.

10.1073/pnas.050658010216199517PMC1239896
14

van der Fits L, Mourits S, Voerman JS, Kant M, Boon L, Laman JD, et al. Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol. 2009;182(9):5836-5845.

10.4049/jimmunol.080299919380832
15

Kim HJ, Jang J, Na K, Lee EH, Gu HJ, Lim YH, et al. TLR7-dependent eosinophil degranulation links psoriatic skin inflammation to small intestinal inflammatory changes in mice. Exp Mol Med. 2024;56:1164-1177.

10.1038/s12276-024-01225-y38689088PMC11148187
16

Johnston DGW, Hambly R, Kearney N, Tobin DJ, Kirby B. A preliminary study of soluble CD14 levels in the serum of patients with hidradenitis suppurativa as a marker of "leaky gut". HRP Open Res. 2022;5(68):1-8.

10.12688/hrbopenres.13633.1
17

Jang J, Hwang S, Oh AR, Park S, Yaseen U, Kim JG, et al. Fructose malabsorption in ChREBP-deficient mice disrupts the small intestine immune microenvironment and leads to diarrhea-dominant bowel habit changes. Inflamm Res. 2023;72(4):769-782.

10.1007/s00011-023-01707-136813915
18

De Pessemier B, Grine L, Debaere M, Maes A, Paetzold B, Callewaert C. Gut-Skin Axis: Current Knowledge of the Interrelationship between Microbial Dysbiosis and Skin Conditions. Microorganisms. 2021;9(2):353.

10.3390/microorganisms902035333670115PMC7916842
19

Leite GGS, Weitsman S, Parodi G, Celly S, Sedighi R, Sanchez M, et al. Mapping the Segmental Microbiomes in the Human Small Bowel in Comparison with Stool: A REIMAGINE Study. Dig Dis Sci. 2020;65(9):2595-2604.

10.1007/s10620-020-06173-x32140945PMC7419378
20

Christ A, Günther P, Lauterbach MAR, Duewell P, Biswas D, Pelka K, et al. Western Diet Triggers NLRP3-Dependent Innate Immune Reprogramming. Cell. 2018;172(1-2):162-175.e14.

10.1016/j.cell.2017.12.01329328911PMC6324559
21

Amaral FA, Costa VV, Tavares LD, Sachs D, Coelho FM, Fagundes CT, et al. NLRP3 inflammasome-mediated neutrophil recruitment and hypernociception depend on leukotriene B(4) in a murine model of gout. Arthritis Rheum. 2012;64(2):474-484.

10.1002/art.3335521952942
22

Atkinson FS, Foster-Powell K, Brand-Miller JC. International Tables of Glycemic Index and Glycemic Load Values: 2008. Diabetes Care. 2008;31(12):2281-2183.

10.2337/dc08-123918835944PMC2584181
23

Christ A, Lauterbach M, Latz E. Western Diet and the Immune System: An Inflammatory Connection. Immunity. 2019;51(5):794-811.

10.1016/j.immuni.2019.09.02031747581
24

Park S, Jang J, Kim HJ, Jung Y. Unveiling multifaceted roles of myeloid innate immune cells in the pathogenesis of psoriasis. Mol Aspects Med. 2024;99:101306.

10.1016/j.mam.2024.10130639191143
25

Delgado-Andrade C. Carboxymethyl-lysine: thirty years of investigation in the field of AGE formation. Food Funct. 2016;7(1):46-57.

10.1039/C5FO00918A26462729
26

Bettiga A, Fiorio F, Di Marco F, Trevisani F, Romani A, Porrini E, et al. The Modern Western Diet Rich in Advanced Glycation End-Products (AGEs): An Overview of Its Impact on Obesity and Early Progression of Renal Pathology. Nutrients. 2019;11(8):1748.

10.3390/nu1108174831366015PMC6724323
27

Jena PK, Sheng L, McNeil K, Chau TQ, Yu S, Kiuru M, et al. Long-term Western diet intake leads to dysregulated bile acid signaling and dermatitis with Th2 and Th17 pathway features in mice. J Dermatol Sci. 2019;95(1):13-20.

10.1016/j.jdermsci.2019.05.00731213388PMC6991164
28

Agus A, Denizot J, Thévenot J, Martinez-Medina M, Massier S, Sauvanet P, et al. Western diet induces a shift in microbiota composition enhancing susceptibility to Adherent-Invasive E. coli infection and intestinal inflammation. Sci Rep. 2016;6:19032.

10.1038/srep1903226742586PMC4705701
Information
  • Publisher :The Korean Society for Microbiology and The Korean Society of Virology
  • Publisher(Ko) :대한미생물학회‧대한바이러스학회
  • Journal Title :JOURNAL OF BACTERIOLOGY AND VIROLOGY
  • Volume : 54
  • No :4
  • Pages :367-378
  • Received Date : 2024-10-11
  • Revised Date : 2024-12-02
  • Accepted Date : 2024-12-03
  • DOI :https://doi.org/10.4167/jbv.2024.54.4.367
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