FBXO38 regulates macrophage polarization to control the development of cancer and colitis.
Colitis
FBXO38
Macrophage polarization
Tumor progression
Journal
Cellular & molecular immunology
ISSN: 2042-0226
Titre abrégé: Cell Mol Immunol
Pays: China
ID NLM: 101242872
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
received:
10
01
2023
accepted:
27
08
2023
pmc-release:
01
11
2024
medline:
2
11
2023
pubmed:
12
10
2023
entrez:
11
10
2023
Statut:
ppublish
Résumé
Macrophages are highly plastic cells that differentially regulate multiple pathological conditions, including cancer and autoimmune diseases. In response to various stimuli, macrophages activate different intrinsic signaling pathways and polarize into distinct macrophage subsets. We aimed to identify key new effectors that could control macrophage polarization and impact the development of cancer or colitis. Following treatment with the supernatants of tumor cells, macrophages showed an upregulation in Fbxo38 expression. Subsequently, we further identified that FBXO38 promotes macrophage immunosuppressive function by upregulating the expression of M2-like genes via MAPK and IRF4 signaling without affecting M1-like macrophage polarization. Deletion of Fbxo38 in macrophages was found to block tumor development and protect against DSS-induced colitis. Considering the distinct regulation of tumor development by FBXO38 in T cells and macrophages, we suggest that a comprehensive understanding of FBXO38 function in different cell types is critical for its further translational usage.
Identifiants
pubmed: 37821621
doi: 10.1038/s41423-023-01081-2
pii: 10.1038/s41423-023-01081-2
pmc: PMC10616184
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1367-1378Informations de copyright
© 2023. The Author(s), under exclusive licence to CSI and USTC.
Références
Vesely MD, Zhang T, Chen L. Resistance mechanisms to anti-PD cancer immunotherapy. Annu Rev Immunol. 2022;40:45–74.
doi: 10.1146/annurev-immunol-070621-030155
pubmed: 35471840
Sica A, Erreni M, Allavena P, Porta C. Macrophage polarization in pathology. Cell Mol Life Sci. 2015;72:4111–26.
doi: 10.1007/s00018-015-1995-y
pubmed: 26210152
Boutilier AJ, Elsawa SF. Macrophage polarization states in the tumor microenvironment. Int J Mol Sci. 2021;22:6995.
Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014;41:49–61.
doi: 10.1016/j.immuni.2014.06.010
pubmed: 25035953
pmcid: 4137410
Zhang J, Shi Z, Xu X, Yu Z, Mi J. The influence of microenvironment on tumor immunotherapy. FEBS J. 2019;286:4160–75.
doi: 10.1111/febs.15028
pubmed: 31365790
pmcid: 6899673
Lin Y, Yang X, Yue W, Xu X, Li B, Zou L, et al. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell Mol Immunol. 2014;11:355–66.
doi: 10.1038/cmi.2014.15
pubmed: 24727542
pmcid: 4085517
Zhou X, Li W, Wang S, Zhang P, Wang Q, Xiao J, et al. YAP aggravates inflammatory bowel disease by regulating M1/M2 macrophage polarization and gut microbial homeostasis. Cell Rep. 2019;27:1176–89.e1175.
doi: 10.1016/j.celrep.2019.03.028
pubmed: 31018132
Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol. 2012;2012:718617.
doi: 10.1155/2012/718617
pubmed: 22665990
pmcid: 3361365
Zhao X, Di Q, Liu H, Quan J, Ling J, Zhao Z, et al. MEF2C promotes M1 macrophage polarization and Th1 responses. Cell Mol Immunol. 2022;19:540–53.
doi: 10.1038/s41423-022-00841-w
pubmed: 35194174
pmcid: 8975968
Hunter MM, Wang A, Parhar KS, Johnston MJ, Van Rooijen N, Beck PL, et al. In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology. 2010;138:1395–405.
doi: 10.1053/j.gastro.2009.12.041
pubmed: 20044996
Weisser SB, Brugger HK, Voglmaier NS, McLarren KW, van Rooijen N, Sly LM. SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis. J Leukoc Biol. 2011;90:483–92.
doi: 10.1189/jlb.0311124
pubmed: 21685246
Sumner CJ, d’Ydewalle C, Wooley J, Fawcett KA, Hernandez D, Gardiner AR, et al. A dominant mutation in FBXO38 causes distal spinal muscular atrophy with calf predominance. Am J Hum Genet. 2013;93:976–83.
doi: 10.1016/j.ajhg.2013.10.006
pubmed: 24207122
pmcid: 3824115
Akcimen F, Vural A, Durmus H, Cakar A, Houlden H, Parman YG, et al. A novel homozygous FBXO38 variant causes an early-onset distal hereditary motor neuronopathy type IID. J Hum Genet. 2019;64:1141–4.
doi: 10.1038/s10038-019-0652-y
pubmed: 31420593
Saferali A, Yun JH, Parker MM, Sakornsakolpat P, Chase RP, Lamb A, et al. Analysis of genetically driven alternative splicing identifies FBXO38 as a novel COPD susceptibility gene. PLoS Genet. 2019;15:e1008229.
doi: 10.1371/journal.pgen.1008229
pubmed: 31269066
pmcid: 6634423
Shang D, Dong L, Zeng L, Yang R, Xu J, Wu Y, et al. Two-stage comprehensive evaluation of genetic susceptibility of common variants in FBXO38, AP3B2 and WHAMM to severe chronic periodontitis. Sci Rep. 2015;5:17882.
doi: 10.1038/srep17882
pubmed: 26643602
pmcid: 4672326
Meng X, Liu X, Guo X, Jiang S, Chen T, Hu Z, et al. FBXO38 mediates PD-1 ubiquitination and regulates anti-tumour immunity of T cells. Nature. 2018;564:130–5.
doi: 10.1038/s41586-018-0756-0
pubmed: 30487606
Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature. 2017;545:495–9.
doi: 10.1038/nature22396
pubmed: 28514441
pmcid: 5931375
Wang Z, Hao C, Zhuang Q, Zhan B, Sun X, Huang J, et al. Excretory/secretory products from trichinella spiralis adult worms attenuated DSS-induced colitis in mice by driving PD-1-mediated M2 macrophage polarization. Front Immunol. 2020;11:563784.
doi: 10.3389/fimmu.2020.563784
pubmed: 33117347
pmcid: 7575908
Zheng X, Xiao J, Jiang Q, Zheng L, Liu C, Dong C, et al. AKT2 reduces IFNbeta1 production to modulate antiviral responses and systemic lupus erythematosus. EMBO J. 2022;41:e108016.
doi: 10.15252/embj.2021108016
pubmed: 35191555
pmcid: 8922272
Zhang Q, He Y, Luo N, Patel SJ, Han Y, Gao R, et al. Landscape and Dynamics of Single Immune Cells in Hepatocellular Carcinoma. Cell. 2019;179:829-45.e20.
doi: 10.1016/j.cell.2019.10.003
pubmed: 31675496
Boland BS, He Z, Tsai MS, Olvera JG, Omilusik KD, Duong HG, et al. Heterogeneity and clonal relationships of adaptive immune cells in ulcerative colitis revealed by single-cell analyses. Sci Immunol. 2020;5:eabb4432.
Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol. 2010;11:936–44.
doi: 10.1038/ni.1920
pubmed: 20729857
Antonsen KW, Hviid CVB, Hagensen MK, Sørensen BS, Møller HJ. Soluble PD-1 (sPD-1) is expressed in human macrophages. Cell Immunol. 2021;369:104435.
Grzywa TM, Sosnowska A, Matryba P, Rydzynska Z, Jasinski M, Nowis D, et al. Myeloid cell-derived arginase in cancer immune response. Front Immunol. 2020;11:938.
doi: 10.3389/fimmu.2020.00938
pubmed: 32499785
pmcid: 7242730
Oft M. IL-10: master switch from tumor-promoting inflammation to antitumor immunity. Cancer Immunol Res. 2014;2:194–9.
doi: 10.1158/2326-6066.CIR-13-0214
pubmed: 24778315
Zhang X, Fan L, Wu J, Xu H, Leung WY, Fu K, et al. Macrophage p38alpha promotes nutritional steatohepatitis through M1 polarization. J Hepatol. 2019;71:163–74.
doi: 10.1016/j.jhep.2019.03.014
pubmed: 30914267
Cheng Y, Zhu Y, Xu J, Yang M, Chen P, Xu W, et al. PKN2 in colon cancer cells inhibits M2 phenotype polarization of tumor-associated macrophages via regulating DUSP6-Erk1/2 pathway. Mol Cancer. 2018;17:13.
doi: 10.1186/s12943-017-0747-z
pubmed: 29368606
pmcid: 5784528
Jimenez-Garcia L, Herranz S, Luque A, Hortelano S. Critical role of p38 MAPK in IL-4-induced alternative activation of peritoneal macrophages. Eur J Immunol. 2015;45:273–86.
doi: 10.1002/eji.201444806
pubmed: 25328047
Alam MS, Gaida MM, Ogawa Y, Kolios AG, Lasitschka F, Ashwell JD. Counter-regulation of T cell effector function by differentially activated p38. J Exp Med. 2014;211:1257–70.
doi: 10.1084/jem.20131917
pubmed: 24863062
pmcid: 4042639