1,655
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Formyl peptide receptor-1 (FPR1) represses intestinal oncogenesis

, , , , , , , , , , , , , , , , & ORCID Icon show all
Article: 2237354 | Received 30 Apr 2023, Accepted 12 Jul 2023, Published online: 21 Jul 2023

References

  • Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16(12):713–13. doi:10.1038/s41575-019-0189-8.
  • Kuipers EJ, Grady WM, Lieberman D, Seufferlein T, Sung JJ, Boelens PG, van de Velde CJH, Watanabe T. Colorectal cancer. Nat Rev Dis Primers. 2015;1(1):15065. doi:10.1038/nrdp.2015.65.
  • O’Sullivan DE, Sutherland RL, Town S, Chow K, Fan J, Forbes N, Heitman SJ, Hilsden RJ, Brenner DR. Risk factors for early-onset colorectal cancer: A systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2022;20(6):1229–1240.e5. doi:10.1016/j.cgh.2021.01.037.
  • Morgan E, Arnold M, Gini A, Lorenzoni V, Cabasag CJ, Laversanne M, Vignat J, Ferlay J, Murphy N, Bray F, et al. Global burden of colorectal cancer in 2020 and 2040: incidence and mortality estimates from GLOBOCAN. Gut. 2023;72(2):338–344. doi:10.1136/gutjnl-2022-327736.
  • Vacchelli E, Le Naour J, Kroemer G. The ambiguous role of FPR1 in immunity and inflammation. Oncoimmunology. 2020;9(1):1760061. doi:10.1080/2162402X.2020.1760061.
  • Tucker EJ, Hershman SG, Kohrer C, Belcher-Timme CA, Patel J, Goldberger OA, Christodoulou J, Silberstein J, McKenzie M, Ryan M, et al. Mutations in MTFMT underlie a human disorder of formylation causing impaired mitochondrial translation. Cell Metab. 2011;14(3):428–434. doi:10.1016/j.cmet.2011.07.010.
  • Zhuang Y, Wang L, Guo J, Sun D, Wang Y, Liu W, Xu HE, Zhang C. Molecular recognition of formylpeptides and diverse agonists by the formylpeptide receptors FPR1 and FPR2. Nat Commun. 2022;13(1):1054. doi:10.1038/s41467-022-28586-0.
  • Sun R, Iribarren P, Zhang N, Zhou Y, Gong W, Cho EH, Lockett S, Chertov O, Bednar F, Rogers TJ, et al. Identification of neutrophil granule protein cathepsin G as a novel chemotactic agonist for the G protein-coupled formyl peptide receptor. J Immunol. 2004;173(1):428–436. doi:10.4049/jimmunol.173.1.428.
  • Wang W, Li T, Wang X, Yuan W, Cheng Y, Zhang H, Xu E, Zhang Y, Shi S, Ma D, et al. FAM19A4 is a novel cytokine ligand of formyl peptide receptor 1 (FPR1) and is able to promote the migration and phagocytosis of macrophages. Cell Mol Immunol. 2015;12(5):615–624. doi:10.1038/cmi.2014.61.
  • Baracco EE, Stoll G, Van Endert P, Zitvogel L, Vacchelli E, Kroemer G. Contribution of annexin A1 to anticancer immunosurveillance. Oncoimmunology. 2019;8(11):e1647760. doi:10.1080/2162402X.2019.1647760.
  • Vacchelli E, Ma Y, Baracco EE, Sistigu A, Enot DP, Pietrocola F, Yang H, Adjemian S, Chaba K, Semeraro M, et al. Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science. 2015;350(6263):972–978. doi:10.1126/science.aad0779.
  • Vacchelli E, Enot DP, Pietrocola F, Zitvogel L, Kroemer G. Impact of pattern recognition receptors on the prognosis of breast cancer patients undergoing adjuvant chemotherapy. Cancer Res. 2016;76(11):3122–3126. doi:10.1158/0008-5472.CAN-16-0294.
  • Chiang SF, Huang KC, Chen WT, Chen TW, Ke TW, Chao KSC. An independent predictor of poor prognosis in locally advanced rectal cancer: rs867228 in formyl peptide receptor 1 (FPR1). Oncoimmunology. 2021;10(1):1926074. doi:10.1080/2162402X.2021.1926074.
  • Chiang SF, Huang KC, Chen WT, Chen TW, Ke TW, Chao KSC. Polymorphism of formyl peptide receptor 1 (FPR1) reduces the therapeutic efficiency and antitumor immunity after neoadjuvant chemoradiotherapy (CCRT) treatment in locally advanced rectal cancer. Cancer Immunol Immunother. 2021;70(10):2937–2950. doi:10.1007/s00262-021-02894-8.
  • Carbonnier V, Le Naour J, Bachelot T, Vacchelli E, Andre F, Delaloge S, Kroemer G. Rs867228 in FPR1 accelerates the manifestation of luminal B breast cancer. Oncoimmunology. 2023;12(1):2189823. doi:10.1080/2162402X.2023.2189823.
  • Le Naour J, Liu P, Zhao L, Adjemian S, Sztupinszki Z, Taieb J, Mulot C, Silvin A, Dutertre C-A, Ginhoux F, et al. A TLR3 ligand reestablishes chemotherapeutic responses in the context of FPR1 deficiency. Cancer Discov. 2021;11(2):408–423. doi:10.1158/2159-8290.CD-20-0465.
  • Sztupinszki Z, Le Naour J, Vacchelli E, Laurent-Puig P, Delaloge S, Szallasi Z, Kroemer G. A major genetic accelerator of cancer diagnosis: rs867228 in FPR1. Oncoimmunology. 2021;10(1):1859064. doi:10.1080/2162402X.2020.1859064.
  • Ma Y, Adjemian S, Yang H, Catani JP, Hannani D, Martins I, Michaud M, Kepp O, Sukkurwala AQ, Vacchelli E, et al. ATP-dependent recruitment, survival and differentiation of dendritic cell precursors in the tumor bed after anticancer chemotherapy. Oncoimmunology. 2013;2(6):e24568. doi:10.4161/onci.24568.
  • Angelou A, Andreatos N, Antoniou E, Zacharioudaki A, Theodoropoulos G, Damaskos C, Garmpis N, Yuan C, Xiao W, Theocharis S, et al. A novel modification of the AOM/DSS model for inducing intestinal adenomas in mice. Anticancer Res. 2018;38(6):3467–3470. doi:10.21873/anticanres.12616.
  • Parang B, Barrett CW, Williams CS. AOM/DSS model of colitis-associated cancer. Methods Mol Biol. 2016;1422:297–307.
  • Robertson SJ, Lemire P, Maughan H, Goethel A, Turpin W, Bedrani L, Guttman DS, Croitoru K, Girardin SE, Philpott DJ, et al. Comparison of co-housing and littermate methods for microbiota standardization in mouse models. Cell Rep. 2019;27(6):1910–1919.e2. doi:10.1016/j.celrep.2019.04.023.
  • Li SQ, Su N, Gong P, Zhang HB, Liu J, Wang D, Sun Y-P, Zhang Y, Qian F, Zhao B, et al. The expression of formyl peptide receptor 1 is correlated with tumor invasion of human colorectal cancer. Sci Rep. 2017;7(1):5918. doi:10.1038/s41598-017-06368-9.
  • Moser AR, Luongo C, Gould KA, McNeley MK, Shoemaker AR, Dove WF. ApcMin: a mouse model for intestinal and mammary tumorigenesis. Eur J Cancer. 1995;31(7–8):1061–1064. doi:10.1016/0959-8049(95)00181-H.
  • Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science. 1992;256(5057):668–670. doi:10.1126/science.1350108.
  • Fletcher R, Tong J, Risnik D, Leibowitz BJ, Wang YJ, Concha-Benavente F, DeLiberty JM, Stolz DB, Pai RK, Ferris RL, et al. Non-steroidal anti-inflammatory drugs induce immunogenic cell death in suppressing colorectal tumorigenesis. Oncogene. 2021;40(11):2035–2050. doi:10.1038/s41388-021-01687-8.
  • Goldberg Y, Nassif II, Pittas A, Tsai LL, Dynlacht DB, Rigas B, Shiff SJ. The anti-proliferative effect of sulindac and sulindac sulfide on HT-29 colon cancer cells: alterations in tumor suppressor and cell cycle-regulatory proteins. Oncogene. 1996;12:893–901.
  • Haanen C. Sulindac and its derivatives: a novel class of anticancer agents. Curr Opin Investig Drugs. 2001;2:677–683.
  • Lee HJ, Wang XN, Shi DL, Zheng JJ. Sulindac inhibits canonical Wnt signaling by blocking the PDZ domain of the protein Dishevelled. Angew Chem Int Ed Engl. 2009;48(35):6448–6452. doi:10.1002/anie.200902981.
  • Oldekamp S, Pscheidl S, Kress E, Soehnlein O, Jansen S, Pufe T, Wang JM, Tauber SC, Brandenburg L-O. Lack of formyl peptide receptor 1 and 2 leads to more severe inflammation and higher mortality in mice with of pneumococcal meningitis. Immunology. 2014;143(3):447–461. doi:10.1111/imm.12324.
  • Zhang M, Gao JL, Chen K, Yoshimura T, Liang W, Gong W, Li X, Huang J, McDermott DH, Murphy PM, et al. A critical role of formyl peptide receptors in host defense against Escherichia coli. J Immunol. 2020;204(9):2464–2473. doi:10.4049/jimmunol.1900430.
  • Osei-Owusu P, Charlton TM, Kim HK, Missiakas D, Schneewind O. FPR1 is the plague receptor on host immune cells. Nature. 2019;574(7776):57–62. doi:10.1038/s41586-019-1570-z.
  • Giebeler A, Streetz KL, Soehnlein O, Neumann U, Wang JM, Brandenburg LO, Mukhopadhyay P. Deficiency of formyl peptide receptor 1 and 2 is associated with increased inflammation and enhanced liver injury after LPS-stimulation. PLoS One. 2014;9(6):e100522. doi:10.1371/journal.pone.0100522.
  • Bihler K, Kress E, Esser S, Nyamoya S, Tauber SC, Clarner T, Stope MB, Pufe T, Brandenburg L-O. Formyl peptide receptor 1-mediated glial cell activation in a mouse model of cuprizone-induced demyelination. J Mol Neurosci. 2017;62(2):232–243. doi:10.1007/s12031-017-0924-y.
  • Fusco R, Gugliandolo E, Siracusa R, Scuto M, Cordaro M, D’Amico R, Evangelista M, Peli A, Peritore AF, Impellizzeri D, et al. Formyl peptide receptor 1 signaling in acute inflammation and neural differentiation induced by traumatic brain injury. Biology (Basel). 2020;9(9):238. doi:10.3390/biology9090238.
  • Li J, Chordia MD, Zhang Y, Zong H, Pan D, Zuo Z. Critical role of FPR1 in splenocyte migration into brain to worsen inflammation and ischemic brain injury in mice. Theranostics. 2022;12(7):3024–3044. doi:10.7150/thno.57218.
  • Grommes J, Drechsler M, Soehnlein O. CCR5 and FPR1 mediate neutrophil recruitment in endotoxin-induced lung injury. J Innate Immun. 2014;6(1):111–116. doi:10.1159/000353229.
  • Yuan ZC, Zeng N, Liu L, Wang T, Dai LQ, Wang H, Zeng Z-J, Cao Y-F, Zhou Y-F, Xu D, et al. Mitochondrial damage-associated molecular patterns exacerbate lung fluid imbalance via the formyl peptide receptor-1 signaling pathway in acute lung injury. Crit Care Med. 2021;49(1):e53–e62. doi:10.1097/CCM.0000000000004732.
  • Cardini S, Dalli J, Fineschi S, Perretti M, Lungarella G, Lucattelli M. Genetic ablation of the fpr1 gene confers protection from smoking-induced lung emphysema in mice. Am J Respir Cell Mol Biol. 2012;47(3):332–339. doi:10.1165/rcmb.2012-0036OC.
  • Gao L, Zeng N, Yuan Z, Wang T, Chen L, Yang D, Xu D, Wan C, Wen F, Shen Y, et al. Knockout of formyl peptide receptor-1 attenuates cigarette smoke–induced airway inflammation in mice. Front Pharmacol. 2021;12:632225. doi:10.3389/fphar.2021.632225.
  • Leslie J, Millar BJ, Del Carpio Pons A, Burgoyne RA, Frost JD, Barksby BS, Luli S, Scott J, Simpson AJ, Gauldie J, et al. FPR-1 is an important regulator of neutrophil recruitment and a tissue-specific driver of pulmonary fibrosis. JCI Insight. 2020;5(4). doi:10.1172/jci.insight.125937.
  • D’Amico R, Fusco R, Cordaro M, Siracusa R, Peritore AF, Gugliandolo E, Crupi R, Scuto M, Cuzzocrea S, Di Paola R, et al. Modulation of NLRP3 inflammasome through Formyl Peptide Receptor 1 (Fpr-1) pathway as a new therapeutic target in bronchiolitis obliterans syndrome. Int J Mol Sci. 2020;21(6):21. doi:10.3390/ijms21062144.
  • Alam A, Leoni G, Wentworth CC, Kwal JM, Wu H, Ardita CS, Swanson PA, Lambeth JD, Jones RM, Nusrat A, et al. Redox signaling regulates commensal-mediated mucosal homeostasis and restitution and requires formyl peptide receptor 1. Mucosal Immunol. 2014;7(3):645–655. doi:10.1038/mi.2013.84.
  • Farooq SM, Stadnyk AW. Neutrophil infiltration of the colon is independent of the FPR1 yet FPR1 deficient mice show differential susceptibilities to acute versus chronic induced colitis. Dig Dis Sci. 2012;57(7):1802–1812. doi:10.1007/s10620-012-2082-y.
  • Di Paola R, Fusco R, Gugliandolo E, D’Amico R, Cordaro M, Impellizzeri D, Perretti M, Cuzzocrea S. Formyl peptide receptor 1 signalling promotes experimental colitis in mice. Pharmacol Res. 2019;141:591–601. doi:10.1016/j.phrs.2019.01.041.
  • Neufert C, Becker C, Neurath MF. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc. 2007;2(8):1998–2004. doi:10.1038/nprot.2007.279.
  • Wollam J, Riopel M, Xu YJ, Johnson AMF, Ofrecio JM, Ying W, El Ouarrat D, Chan LS, Han AW, Mahmood NA, et al. Microbiota-produced N-Formyl peptide fMLF promotes obesity-induced glucose intolerance. Diabetes. 2019;68(7):1415–1426. doi:10.2337/db18-1307.
  • Terasaki M, Uehara O, Ogasa S, Sano T, Kubota A, Kojima H, Tanaka T, Maeda H, Miyashita K, Mutoh M, et al. Alteration of fecal microbiota by fucoxanthin results in prevention of colorectal cancer in AOM/DSS mice. Carcinogenesis. 2021;42(2):210–219. doi:10.1093/carcin/bgaa100.
  • Molloy MJ, Grainger JR, Bouladoux N, Hand TW, Koo LY, Naik S, Quinones M, Dzutsev A, Gao J-L, Trinchieri G, et al. Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host & Microbe. 2013;14(3):318–328. doi:10.1016/j.chom.2013.08.003.
  • Alam A, Leoni G, Quiros M, Wu H, Desai C, Nishio H, Jones RM, Nusrat A, Neish AS. The microenvironment of injured murine gut elicits a local pro-restitutive microbiota. Nat microbiol. 2016;1(2):15021. doi:10.1038/nmicrobiol.2015.21.
  • Wang F, Cai K, Xiao Q, He L, Xie L, Liu Z. Akkermansia muciniphila administration exacerbated the development of colitis-associated colorectal cancer in mice. J Cancer. 2022;13(1):124–133. doi:10.7150/jca.63578.
  • Wang L, Tang L, Feng Y, Zhao S, Han M, Zhang C, Yuan G, Zhu J, Cao S, Wu Q, et al. A purified membrane protein from Akkermansia muciniphila or the pasteurised bacterium blunts colitis associated tumourigenesis by modulation of CD8 + T cells in mice. Gut. 2020;69(11):1988–1997. doi:10.1136/gutjnl-2019-320105.
  • Chandrasekharan B, Saeedi BJ, Alam A, Houser M, Srinivasan S, Tansey M, Jones R, Nusrat A, Neish AS. Interactions between commensal bacteria and enteric neurons, via FPR1 induction of ROS, increase gastrointestinal motility in mice. Gastroenterology. 2019;157(1):179–192.e2. doi:10.1053/j.gastro.2019.03.045.
  • Hattori N, Niwa T, Ishida T, Kobayashi K, Imai T, Mori A, Kimura K, Mori T, Asami Y, Ushijima T, et al. Antibiotics suppress colon tumorigenesis through inhibition of aberrant DNA methylation in an azoxymethane and dextran sulfate sodium colitis model. Cancer Sci. 2019;110:147–156. doi:10.1111/cas.13880.
  • Lee JG, Eun CS, Jo SV, Lee AR, Park CH, Han DS, Nakano H. The impact of gut microbiota manipulation with antibiotics on colon tumorigenesis in a murine model. PLoS One. 2019;14(12):e0226907. doi:10.1371/journal.pone.0226907.
  • Xu H, Hiraishi K, Kurahara LH, Nakano-Narusawa Y, Li X, Hu Y, Matsuda Y, Zhang H, Hirano K. Inhibitory effects of breast milk-derived lactobacillus rhamnosus Probio-M9 on colitis-associated carcinogenesis by restoration of the gut microbiota in a mouse model. Nutrients. 2021;13(4):1143. doi:10.3390/nu13041143.
  • Enot DP, Vacchelli E, Jacquelot N, Zitvogel L, Kroemer G. TumGrowth: An open-access web tool for the statistical analysis of tumor growth curves. Oncoimmunology. 2018;7(9):e1462431. doi:10.1080/2162402X.2018.1462431.
  • Le Naour J, Montegut L, Joseph A, Garbin K, Vacchelli E, Kroemer G, Pol JG, Maiuri MC. Improved Swiss-rolling method for histological analyses of colon tissue. MethodsX. 2022;9:101630. doi:10.1016/j.mex.2022.101630.
  • Bankhead P, Loughrey MB, Fernandez JA, Dombrowski Y, McArt DG, Dunne PD, McQuaid S, Gray RT, Murray LJ, Coleman HG, et al. QuPath: Open source software for digital pathology image analysis. Sci Rep. 2017;7(1):16878. doi:10.1038/s41598-017-17204-5.
  • Boivin GP, Washington K, Yang K, Ward JM, Pretlow TP, Russell R, Besselsen DG, Godfrey VL, Doetschman T, Dove WF, et al. Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology. 2003;124(3):762–777. doi:10.1053/gast.2003.50094.
  • Nolte T, Brander-Weber P, Dangler C, Deschl U, Elwell MR, Greaves P, Hailey R, Leach MW, Pandiri AR, Rogers A, et al. Nonproliferative and proliferative lesions of the gastrointestinal tract, pancreas and salivary glands of the rat and mouse. J Toxicol Pathol. 2016;29(1_Suppl):1S–125S. doi:10.1293/tox.29.1S.
  • Ward JM, Treuting PM. Rodent intestinal epithelial carcinogenesis: pathology and preclinical models. Toxicol Pathol. 2014;42(1):148–161. doi:10.1177/0192623313505156.
  • Angelakis E, Bachar D, Henrissat B, Armougom F, Audoly G, Lagier JC, Robert C, Raoult D. Glycans affect DNA extraction and induce substantial differences in gut metagenomic studies. Sci Rep. 2016;6(1):26276. doi:10.1038/srep26276.
  • Boudreau J, Koshy S, Cummings D, Wan Y. Culture of myeloid dendritic cells from bone marrow precursors. J Vis Exp. 2008;17. doi:10.3791/769-v.