Study of dietary‑induced progression of psoriasis‑like mice based on gut macrophage polarization

Zeng,Wucheng; Wang,Yihan; Cao,Yi; Xing,Fengling; Yang,Xiaohong

doi:10.3892/etm.2023.11976

Study of dietary‑induced progression of psoriasis‑like mice based on gut macrophage polarization

Authors:
- Wucheng Zeng
- Yihan Wang
- Yi Cao
- Fengling Xing
- Xiaohong Yang
View Affiliations

Affiliations: Department of Dermatology and Venereology, Hangzhou TCM Hospital Affiliated to Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310007, P.R. China, Department of Dermatology, Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310053, P.R. China, Department of Dermatology, The First Affiliated Hospital of Zhejiang Chinese Medical University, Zhejiang Hangzhou, Zhejiang 310006, P.R. China, Department of Dermatology and Venereology, Hangzhou TCM Hospital Affiliated to Zhejiang Chinese Medical University, Hangzhou, Zhejiang 310007, P.R. China
Published online on: April 24, 2023 https://doi.org/10.3892/etm.2023.11976
Article Number: 278
Copyright: © Zeng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The aim of the present study was to investigate the influence of stimulating food (SF), a Traditional Chinese Medicine term for a high protein, high fat diet, on psoriasis exacerbation. It was hypothesized that SF disposed psoriasis‑like aggravation might be related to inflammatory pathways induction via gut dysbiosis. In the present study, mice were fed either an SF or normal diet for 4 weeks. In the last week, their back hair was removed to establish psoriasis‑like dermatitis by imiquimod. After sacrifice, blood samples, alimentary tissues and skin lesions were collected and tested by enzyme‑linked immunosorbent assay, western blotting, immunohistochemistry and immunofluorescence. Compared with normal diet groups, body weight and blood glucose of SF diet mice were not increased, but they exhibited higher modified Psoriasis Area and Severity Index scores and corresponding epithelial hyperproliferation. Unexpectedly, skin lesions showed abnormal lower protein expressions of Notch and TLR‑2/NF‑κB p65 signaling pathway, which was attributable to severe skin damage. No difference was observed in the structure and inflammatory cell infiltration of the gut between groups. Instead, macrophage polarization (M1/M2) in the gut of the SF diet group marked by high expression of CD11b (a marker of macrophage, M1) and mild low expression of MRC1 (a marker of macrophage, M2), which resulted in increased TNF‑α, decreased IL‑10, IL‑35, and unchanged IL‑17 in serum. Furthermore, serum derived from SF diet mice promoted translocation of NF‑κB p65 in HaCaT cells, which indirectly suggested a systemic inflammation. These results suggested that mice fed a continuous SF diet for a time could change gut macrophage polarization, which secretes proinflammatory cytokines into blood circulation. Once transported to skin lesions, these cytokines activate psoriasis tissue resident immune cells and present as psoriasis exacerbation.

View Figures

View References

1	Griffiths CEM, Armstrong AW, Gudjonsson JE and Barker JNWN: Psoriasis. Lancet. 397:1301–1315. 2021.PubMed/NCBI View Article : Google Scholar
2	Takeshita J, Grewal S, Langan SM, Mehta NN, Ogdie A, Van Voorhees AS and Gelfand JM: Psoriasis and comorbid diseases: Epidemiology. J Am Acad Dermatol. 76:377–390. 2017.PubMed/NCBI View Article : Google Scholar
3	Madden SK, Flanagan KL and Jones G: How lifestyle factors and their associated pathogenetic mechanisms impact psoriasis. Clin Nutr. 39:1026–1040. 2020.PubMed/NCBI View Article : Google Scholar
4	Zhu FY and Xie GQ: Discussion on Chinese Medicine Diet taboo-fawu. Chinese Journal of Traditional Chinese Medicine and Pharmacy. 7:3104–3106. 2018.
5	Yu S, Wu X, Zhou Y, Sheng L, Jena PK, Han D, Wan YJY and Hwang ST: 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. 139:1404–1407. 2019.PubMed/NCBI View Article : Google Scholar
6	Boericke H: Critical considerations on a new treatment for psoriasis. Dtsch Gesundheitsw. 7:919–922. 1952.PubMed/NCBI(In German).
7	Petrozzi JW and Rosenbloom J: Low-tryptophan diet in treatment of psoriasis. JAMA. 205:345–346. 1968.PubMed/NCBI
8	Zackheim HS and Farber EM: Low-protein diet and psoriasis. A hospital study. Arch Dermatol. 99:580–586. 1969.PubMed/NCBI
9	Kragballe K and Fogh K: A low-fat diet supplemented with dietary fish oil (Max-EPA) results in improvement of psoriasis and in formation of leukotriene B5. Acta Derm Venereol. 69:23–28. 1989.PubMed/NCBI
10	Adawi M, Damiani G, Bragazzi NL, Bridgewood C, Pacifico A, Conic RRZ, Morrone A, Malagoli P, Pigatto PDM, Amital H, et al: The impact of intermittent fasting (Ramadan Fasting) on psoriatic arthritis disease activity, enthesitis, and dactylitis: A multicentre study. Nutrients. 11(601)2019.PubMed/NCBI View Article : Google Scholar
11	Passali M, Josefsen K, Frederiksen JL and Antvorskov JC: Current evidence on the efficacy of gluten-free diets in multiple sclerosis, psoriasis, type 1 diabetes and autoimmune thyroid diseases. Nutrients. 12(2316)2020.PubMed/NCBI View Article : Google Scholar
12	Spiera H and Lefkovits AM: Turkey, tryptophan, and psoriasis. Lancet. 2(1418)1967.PubMed/NCBI View Article : Google Scholar
13	Phan C, Touvier M, Kesse-Guyot E, Adjibade M, Hercberg S, Wolkenstein P, Chosidow O, Ezzedine K and Sbidian E: Association between mediterranean anti-inflammatory dietary profile and severity of psoriasis: Results from the NutriNet-Santé cohort. JAMA Dermatol. 154:1017–1024. 2018.PubMed/NCBI View Article : Google Scholar
14	Balić A, Vlašić D, Žužul K, Marinović B and Mokos ZB: Omega-3 versus omega-6 polyunsaturated fatty acids in the prevention and treatment of inflammatory skin diseases. Int J Mol Sci. 21(741)2020.PubMed/NCBI View Article : Google Scholar
15	Barrea L, Savanelli MC, Di Somma C, Napolitano M, Megna M, Colao A and Savastano S: Vitamin D and its role in psoriasis: An overview of the dermatologist and nutritionist. Rev Endocr Metab Disord. 18:195–205. 2017.PubMed/NCBI View Article : Google Scholar
16	Millsop JW, Bhatia BK, Debbaneh M, Koo J and Liao W: Diet and psoriasis, part III: Role of nutritional supplements. J Am Acad Dermatol. 71:561–569. 2014.PubMed/NCBI View Article : Google Scholar
17	Chen W, Zhou X and Zhu W: Trace elements homeostatic imbalance in psoriasis: A meta-analysis. Biol Trace Elem Res. 191:313–322. 2019.PubMed/NCBI View Article : Google Scholar
18	Ely PH: Is psoriasis a bowel disease? Successful treatment with bile acids and bioflavonoids suggests it is. Clin Dermatol. 36:376–389. 2018.PubMed/NCBI View Article : Google Scholar
19	Zackheim HS: Taurine and diet in psoriasis. Arch Dermatol. 118(961)1982.PubMed/NCBI
20	Reich K, Augustin M, Thaçi D, Pinter A, Leutz A, Henneges C, Schneider E, Schacht A, Dossenbach M and Mrowietz U: A 24-week multicentre, randomized, open-label, parallel-group study comparing the efficacy and safety of ixekizumab vs. fumaric acid esters and methotrexate in patients with moderate-to-severe plaque psoriasis naive to systemic treatment. Br J Dermatol. 182:869–879. 2020.PubMed/NCBI View Article : Google Scholar
21	Jena PK, Sheng L, McNeil K, Chau TQ, Yu S, Kiuru M, Fung MA, Hwang ST and Wan YJY: Long-term Western diet intake leads to dysregulated bile acid signaling and dermatitis with Th2 and Th17 pathway features in mice. J Dermatol Sci. 95:13–20. 2019.PubMed/NCBI View Article : Google Scholar
22	Yu S, Wu X, Shi Z, Huynh M, Jena PK, Sheng L, Zhou Y, Han D, Wan YJY and Hwang ST: Diet-induced obesity exacerbates imiquimod-mediated psoriasiform dermatitis in anti-PD-1 antibody-treated mice: Implications for patients being treated with checkpoint inhibitors for cancer. J Dermatol Sci. 97:194–200. 2020.PubMed/NCBI View Article : Google Scholar
23	Fernández-Armenteros JM, Gómez-Arbonés X, Buti-Soler M, Betriu-Bars A, Sanmartin-Novell V, Ortega-Bravo M, Martínez-Alonso M, Garí E, Portero-Otín M, Santamaria-Babi L and Casanova-Seuma JM: Psoriasis, metabolic syndrome and cardiovascular risk factors. A population-based study. J Eur Acad Dermatol Venereol. 33:128–135. 2019.PubMed/NCBI View Article : Google Scholar
24	Mahil SK, McSweeney SM, Kloczko E, McGowan B, Barker JN and Smith CH: Does weight loss reduce the severity and incidence of psoriasis or psoriatic arthritis? A critically appraised topic. Br J Dermatol. 181:946–953. 2019.PubMed/NCBI View Article : Google Scholar
25	De Angelis M, Garruti G, Minervini F, Bonfrate L, Portincasa P and Gobbetti M: The food-gut human axis: The effects of diet on gut microbiota and metabolome. Curr Med Chem. 26:3567–3583. 2019.PubMed/NCBI View Article : Google Scholar
26	Gentile CL and Weir TL: The gut microbiota at the intersection of diet and human health. Science. 362:776–780. 2018.PubMed/NCBI View Article : Google Scholar
27	Tran HQ, Bretin A, Adeshirlarijaney A, Yeoh BS, Vijay-Kumar M, Zou J, Denning TL, Chassaing B and Gewirtz AT: ‘Western Diet’-induced adipose inflammation requires a complex gut microbiota. Cell Mol Gastroenterol Hepatol. 9:313–333. 2020.PubMed/NCBI View Article : Google Scholar
28	Ye C, Yano H, Workman CJ and Vignali DAA: Interleukin-35: Structure, function and its impact on immune-related diseases. J Interferon Cytokine Res. 41:391–406. 2021.PubMed/NCBI View Article : Google Scholar
29	Yang BY, Cheng YG, Liu Y, Liu Y, Tan JY, Guan W, Guo S and Kuang HX: Datura Metel L. Ameliorates imiquimod-induced psoriasis-like dermatitis and inhibits inflammatory cytokines production through TLR7/8-MyD88-NF-κB-NLRP3 inflammasome pathway. Molecules. 24(2157)2019.PubMed/NCBI View Article : Google Scholar
30	Marasca C, Scala E, Di Caprio R, Raimondo A, Cacciapuoti S, Balato A and Fabbrocini G: Notch dysregulation and hidradenitis suppurativa, psoriasis, atopic dermatitis and lichen planus: Let's talk about Numb. Br J Dermatol. 180:950–951. 2019.PubMed/NCBI View Article : Google Scholar
31	Kashem SW, Haniffa M and Kaplan DH: Antigen-presenting cells in the skin. Annu Rev Immunol. 35:469–499. 2017.PubMed/NCBI View Article : Google Scholar
32	Kim ES, Han K, Kim MK, Park YM, Baek KH, Moon SD, Han JH, Song KH and Kwon HS: Impact of metabolic status on the incidence of psoriasis: A Korean nationwide cohort study. Sci Rep. 7(1989)2017.PubMed/NCBI View Article : Google Scholar
33	Semenov YR, Herbosa CM, Rogers AT, Huang A, Kwatra SG, Cohen B, Anadkat MJ and Silverberg JI: Psoriasis and mortality in the United States: Data from the national health and nutrition examination survey. J Am Acad Dermatol. 85:396–403. 2021.PubMed/NCBI View Article : Google Scholar
34	Mohammadi A, Blesso CN, Barreto GE, Banach M, Majeed M and Sahebkar A: Macrophage plasticity, polarization and function in response to curcumin, a diet-derived polyphenol, as an immunomodulatory agent. J Nutr Biochem. 66:1–16. 2019.PubMed/NCBI View Article : Google Scholar
35	Brembilla NC, Senra L and Boehncke WH: The IL-17 family of cytokines in psoriasis: IL-17A and beyond. Front Immunol. 9(1682)2018.PubMed/NCBI View Article : Google Scholar
36	Yilmaz SB, Cicek N, Coskun M, Yegin O and Alpsoy E: Serum and tissue levels of IL-17 in different clinical subtypes of psoriasis. Arch Dermatol Res. 304:465–469. 2012.PubMed/NCBI View Article : Google Scholar
37	De Simone C, Dapavo P, Malagoli P, Martella A, Campanati A, Campione E, Errichetti E, Franchi C, Gambardella A, Megna M, et al: Long-term proactive management of psoriasis with calcipotriol and betamethasone dipropionate foam: An Italian consensus through a combined nominal group technique and Delphi approach. Int J Dermatol. 61:1543–1551. 2022.PubMed/NCBI View Article : Google Scholar
38	Benhadou F, Mintoff D and Del Marmol V: Psoriasis: Keratinocytes or immune cells-which is the trigger? Dermatology. 235:91–100. 2019.PubMed/NCBI View Article : Google Scholar
39	Thatikonda S, Pooladanda V, Sigalapalli DK and Godugu C: Piperlongumine regulates epigenetic modulation and alleviates psoriasis-like skin inflammation via inhibition of hyperproliferation and inflammation. Cell Death Dis. 11(21)2020.PubMed/NCBI View Article : Google Scholar
40	Siebel C and Lendahl U: Notch signaling in development, tissue homeostasis, and disease. Physiol Rev. 97:1235–1294. 2017.PubMed/NCBI View Article : Google Scholar
41	National Psoriasis Epidemic Survey Group. Distribution of psoriasis in China: A nation-wide screening in 1984. J Dermatol Venereol. 11:66–78. 1989.
42	Qiao J, Jia QN, Li F, He CX, Wu C, Yu XL, et al: Epidemic Analysis of Dietary Risk Factors for Psoriasis Vulgaris. The Chinese Journal of Dermatovenereology,. 31:1301–1305. 2017.
43	Xu Y, Yang J and Yang L: Research on social phenomenon of Chinese dining tables. Sci Technol Information. 10:241–242. 2011.