Dietary iron modulates gut microbiota and induces SLPI secretion to promote colorectal tumorigenesis

References

• Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–20. PMID:35020204. doi:10.3322/caac.21708.
   PubMed Web of Science ®Google Scholar
• Casari S, Di Paola M, Banci E, Diallo S, Scarallo L, Renzo S, Gori A, Renzi S, Paci M, de Mast Q, et al. Changing dietary habits: the impact of urbanization and rising socio-economic status in families from Burkina Faso in Sub-Saharan Africa. Nutrients. 2022;14(9):1782. PMID:35565752. doi:10.3390/nu14091782.
   PubMed Web of Science ®Google Scholar
• Kumar GS, Kulkarni M, Rathi N. Evolving food choices among the urban Indian middle-class: a qualitative study. Front Nutr. 2022;9:844413. PMID:35425799. doi:10.3389/fnut.2022.844413.
   PubMed Web of Science ®Google Scholar
• da Costa GG, da Conceicao Nepomuceno G, da Silva Pereira A, Simoes BFT. Worldwide dietary patterns and their association with socioeconomic data: an ecological exploratory study. Global Health. 2022;18(1):31. PMID:35279165. doi:10.1186/s12992-022-00820-w.
   PubMed Web of Science ®Google Scholar
• Keum N, Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16(12):713–732. PMID:31455888. doi:10.1038/s41575-019-0189-8.
   PubMed Web of Science ®Google Scholar
• Beyaz S, Mana MD, Roper J, Kedrin D, Saadatpour A, Hong SJ, Bauer-Rowe KE, Xifaras ME, Akkad A, Arias E, et al. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature. 2016;531(7592):53–58. PMID:26935695. doi:10.1038/nature17173.
   PubMed Web of Science ®Google Scholar
• Gurjao C, Zhong R, Haruki K, Li YY, Spurr LF, Lee-Six H, Reardon B, Ugai T, Zhang X, Cherniack AD, et al. Discovery and features of an alkylating signature in colorectal cancer. Cancer Discov. 2021;11(10):2446–2455. doi:10.1158/2159-8290.CD-20-1656.
   PubMed Web of Science ®Google Scholar
• Yang J, Wei H, Zhou Y, Szeto CH, Li C, Lin Y, Coker OO, Lau HCH, Chan AWH, Sung JJY, et al. High-fat diet promotes colorectal tumorigenesis through modulating gut microbiota and metabolites. Gastroenterology. 2022;162(1):135–149.e2. PMID:34461052. doi:10.1053/j.gastro.2021.08.041.
   PubMed Web of Science ®Google Scholar
• Beyaz S, Chung C, Mou H, Bauer-Rowe KE, Xifaras ME, Ergin I, Dohnalova L, Biton M, Shekhar K, Eskiocak O, et al. Dietary suppression of MHC class II expression in intestinal epithelial cells enhances intestinal tumorigenesis. Cell Stem Cell. 2021;28(11):1922–1935.e5. PMID:34529935. doi:10.1016/j.stem.2021.08.007.
   PubMed Web of Science ®Google Scholar
• Kabat GC, Miller AB, Jain M, Rohan TE. A cohort study of dietary iron and heme iron intake and risk of colorectal cancer in women. Br J Cancer. 2007;97(1):118–122. PMID:17551493. doi:10.1038/sj.bjc.6603837.
   PubMed Web of Science ®Google Scholar
• Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, Flanders WD, Rodriguez C, Sinha R, Calle EE. Meat consumption and risk of colorectal cancer. JAMA. 2005;293(2):172–182. PMID:15644544. doi:10.1001/jama.293.2.172.
   PubMed Web of Science ®Google Scholar
• Nowell S, Coles B, Sinha R, MacLeod S, Luke Ratnasinghe D, Stotts C, Kadlubar FF, Ambrosone CB, Lang NP. Analysis of total meat intake and exposure to individual heterocyclic amines in a case-control study of colorectal cancer: contribution of metabolic variation to risk. Mutat Res. 2002;506-507:175–185. PMID:12351157. doi:10.1016/s0027-51070200164-1.
   PubMed Web of Science ®Google Scholar
• Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Gammon MD, Ammerman AS, Sandler RS. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol. 2003;157(5):434–445. PMID:12615608. doi:10.1093/aje/kwf221.
   PubMed Web of Science ®Google Scholar
• Larsson SC, Rafter J, Holmberg L, Bergkvist L, Wolk A. Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer. 2005;113(5):829–834. PMID:15499619. doi:10.1002/ijc.20658.
   PubMed Web of Science ®Google Scholar
• Lescinsky H, Afshin A, Ashbaugh C, Bisignano C, Brauer M, Ferrara G, Hay SI, He J, Iannucci V, Marczak LB, et al. Health effects associated with consumption of unprocessed red meat: a Burden of Proof study. Nat Med. 2022;28(10):2075–2082. PMID:36216940. doi:10.1038/s41591-022-01968-z.
   PubMed Web of Science ®Google Scholar
• Farvid MS, Sidahmed E, Spence ND, Mante Angua K, Rosner BA, Barnett JB. Consumption of red meat and processed meat and cancer incidence: a systematic review and meta-analysis of prospective studies. Eur J Epidemiol. 2021;36(9):937–951. PMID:34455534. doi:10.1007/s10654-021-00741-9.
   PubMed Web of Science ®Google Scholar
• Trakman GL, Fehily S, Basnayake C, Hamilton AL, Russell E, Wilson-O’Brien A, Kamm MA. Diet and gut microbiome in gastrointestinal disease. J Gastroenterol Hepatol. 2022;37(2):237–245. PMID:34716949. doi:10.1111/jgh.15728.
   PubMed Web of Science ®Google Scholar
• Garcia-Montero C, Fraile-Martinez O, Gomez-Lahoz AM, Pekarek L, Castellanos AJ, Noguerales-Fraguas F, Coca S, Guijarro LG, Garcia-Honduvilla N, Asunsolo A, et al. Nutritional components in western diet versus Mediterranean diet at the gut microbiota–immune system interplay. Implications Health Dis Nutr. 2021;13(2):699. PMID:33671569. doi:10.3390/nu13020699.
   Google Scholar
• Daou Y, Falabregue M, Pourzand C, Peyssonnaux C, Edeas M. Host and microbiota derived extracellular vesicles: crucial players in iron homeostasis. Front Med (Lausanne). 2022;9:985141. doi:10.3389/fmed.2022.985141.
   PubMed Web of Science ®Google Scholar
• Barone M, D’Amico F, Brigidi P, Turroni S. Gut microbiome-micronutrient interaction: the key to controlling the bioavailability of minerals and vitamins? Biofactors. 2022;48(2):307–314. doi:10.1002/biof.1835.
   PubMed Web of Science ®Google Scholar
• Ellermann M, Arthur JC. Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radic Biol Med. 2017;105:68–78. doi:10.1016/j.freeradbiomed.2016.10.489.
   PubMed Web of Science ®Google Scholar
• Martin P, Tronnet S, Garcie C, Oswald E. Interplay between siderophores and colibactin genotoxin in Escherichia coli. Iubmb Life. 2017;69(6):435–441. PMID:28295919. doi:10.1002/iub.1612.
   PubMed Web of Science ®Google Scholar
• Li L, Li X, Zhong W, Yang M, Xu M, Sun Y, Ma J, Liu T, Song X, Dong W, et al. Gut microbiota from colorectal cancer patients enhances the progression of intestinal adenoma in Apc(min/+) mice. EBio Med. 2019;48:301–315. doi:10.1016/j.ebiom.2019.09.021.
   PubMed Web of Science ®Google Scholar
• Wong SH, Zhao L, Zhang X, Nakatsu G, Han J, Xu W, Xiao X, Kwong TNY, Tsoi H, Wu WKK, et al. Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology. 2017;153(6):1621–1633.e1626. PMID:28823860. doi:10.1053/j.gastro.2017.08.022.
   PubMed Web of Science ®Google Scholar
• Nugteren S, Samsom JN. Secretory Leukocyte Protease Inhibitor (SLPI) in mucosal tissues: protects against inflammation, but promotes cancer. Cytokine Growth Factor Rev. 2021;59:22–35. PMID:33602652. doi:10.1016/j.cytogfr.2021.01.005.
   PubMed Web of Science ®Google Scholar
• Majchrzak-Gorecka M, Majewski P, Grygier B, Murzyn K, Cichy J. Secretory leukocyte protease inhibitor (SLPI), a multifunctional protein in the host defense response. Cytokine Growth Factor Rev. 2016;28:79–93. PMID:26718149. doi:10.1016/j.cytogfr.2015.12.001.
   PubMed Web of Science ®Google Scholar
• Douglas TC, Hannila SS. Working from within: how secretory leukocyte protease inhibitor regulates the expression of pro-inflammatory genes. Biochem Cell Biol. 2022;100(1):1–8. PMID:34555292. doi:10.1139/bcb-2021-0284.
   PubMedGoogle Scholar
• Nukiwa T, Suzuki T, Fukuhara T, Kikuchi T. Secretory leukocyte peptidase inhibitor and lung cancer. Cancer Sci. 2008;99(5):849–855. PMID:18380788. doi:10.1111/j.1349-7006.2008.00772.x.
   PubMed Web of Science ®Google Scholar
• Nugteren S, Goos J, Delis-van Diemen PM, Simons-Oosterhuis Y, Lindenbergh-Kortleve DJ, van Haaften DH, Sanders J, Meijer GA, Fijneman RJA, Samsom JN. Expression of the immune modulator secretory leukocyte protease inhibitor (SLPI) in colorectal cancer liver metastases and matched primary tumors is associated with a poorer prognosis. Oncoimmunology. 2020;9(1):1832761. PMID:33101778. doi:10.1080/2162402X.2020.1832761.
   PubMed Web of Science ®Google Scholar
• Wen J, Nikitakis NG, Chaisuparat R, Greenwell-Wild T, Gliozzi M, Jin W, Adli A, Moutsopoulos N, Wu T, Warburton G, et al. Secretory leukocyte protease inhibitor (SLPI) expression and tumor invasion in oral squamous cell carcinoma. Am J Pathol. 2011;178(6):2866–2878. PMID:21641406. doi:10.1016/j.ajpath.2011.02.017.
   PubMed Web of Science ®Google Scholar
• Nugteren S, den Uil SH, Delis-van Diemen PM, Simons-Oosterhuis Y, Lindenbergh-Kortleve DJ, van Haaften DH, Stockmann H, Sanders J, Meijer GA, Fijneman RJA, et al. High expression of secretory leukocyte protease inhibitor (SLPI) in stage III micro-satellite stable colorectal cancer is associated with reduced disease recurrence. Sci Rep. 2022;12(1):12174. PMID:35842496. doi:10.1038/s41598-022-16427-5.
   PubMed Web of Science ®Google Scholar
• Wei Z, Liu G, Jia R, Zhang W, Li L, Zhang Y, Wang Z, Bai X. Targeting secretory leukocyte protease inhibitor (SLPI) inhibits colorectal cancer cell growth, migration and invasion via downregulation of AKT. Peer J. 2020;8:e9400. PMID:32742768. doi:10.7717/peerj.9400.
   PubMed Web of Science ®Google Scholar
• Sugino T, Yamaguchi T, Ogura G, Kusakabe T, Goodison S, Homma Y, Suzuki T. The secretory leukocyte protease inhibitor (SLPI) suppresses cancer cell invasion but promotes blood-borne metastasis via an invasion-independent pathway. J Pathol. 2007;212(2):152–160. PMID:17455170. doi:10.1002/path.2156.
   PubMed Web of Science ®Google Scholar
• Yang Z, Chen J, Xie H, Liu T, Chen Y, Ma Z, Pei X, Yang W, Li L. Androgen receptor suppresses prostate cancer metastasis but promotes bladder cancer metastasis via differentially altering miRNA525-5p/SLPI-mediated vasculogenic mimicry formation. Cancer Lett. 2020;473:118–129. PMID:31843555. doi:10.1016/j.canlet.2019.12.018.
   PubMed Web of Science ®Google Scholar
• Parang B, Barrett CW, Williams CS. AOM/DSS model of colitis-associated cancer. Methods Mol Biol. 2016;1422:297–307. PMID:27246042. doi:10.1007/978-1-4939-3603-8_26.
   PubMedGoogle Scholar
• Piskin E, Cianciosi D, Gulec S, Tomas M, Capanoglu E. Iron absorption: factors, limitations, and improvement methods. ACS Omega. 2022;7(24):20441–20456. doi:10.1021/acsomega.2c01833. PMID:35755397.
   PubMed Web of Science ®Google Scholar
• Xue X, Ramakrishnan SK, Weisz K, Triner D, Xie L, Attili D, Pant A, Gyorffy B, Zhan M, Carter-Su C, et al. Iron uptake via DMT1 integrates cell cycle with JAK-STAT3 signaling to promote colorectal tumorigenesis. Cell Metab. 2016;24(3):447–461. PMID:27546461. doi:10.1016/j.cmet.2016.07.015.
   PubMed Web of Science ®Google Scholar
• Schwartz AJ, Goyert JW, Solanki S, Kerk SA, Chen B, Castillo C, Hsu PP, Do BT, Singhal R, Dame MK, et al. Hepcidin sequesters iron to sustain nucleotide metabolism and mitochondrial function in colorectal cancer epithelial cells. Nat Metab. 2021;3(7):969–982. PMID:34155415. doi:10.1038/s42255-021-00406-7.
   PubMedGoogle Scholar
• David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. PMID:24336217. doi:10.1038/nature12820.
   PubMed Web of Science ®Google Scholar
• Wong SH, Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol. 2019;16(11):690–704. PMID:31554963. doi:10.1038/s41575-019-0209-8.
   PubMed Web of Science ®Google Scholar
• Ahmad Kendong SM, Raja Ali RA, Nawawi KNM, Ahmad HF, Mokhtar NM. Gut dysbiosis and intestinal barrier dysfunction: potential explanation for early-onset colorectal cancer. Front Cell Infect Microbiol. 2021;11:744606. PMID:34966694. doi:10.3389/fcimb.2021.744606.
   PubMed Web of Science ®Google Scholar
• Genua F, Raghunathan V, Jenab M, Gallagher WM, Hughes DJ. The role of gut barrier dysfunction and microbiome dysbiosis in colorectal cancer development. Front Oncol. 2021;11:626349. PMID:33937029. doi:10.3389/fonc.2021.626349.
   PubMed Web of Science ®Google Scholar
• Ahmad R, Kumar B, Chen Z, Chen X, Muller D, Lele SM, Washington MK, Batra SK, Dhawan P, Singh AB. Loss of claudin-3 expression induces IL6/gp130/Stat3 signaling to promote colon cancer malignancy by hyperactivating Wnt/beta-catenin signaling. Oncogene. 2017;36(47):6592–6604. PMID:28783170. doi:10.1038/onc.2017.259.
   PubMed Web of Science ®Google Scholar
• Li M, Zhao J, Cao M, Liu R, Chen G, Li S, Xie Y, Xie J, Cheng Y, Huang L, et al. Mast cells-derived MiR-223 destroys intestinal barrier function by inhibition of CLDN8 expression in intestinal epithelial cells. Biol Res. 2020;53(1):12. PMID:32209121. doi:10.1186/s40659-020-00279-2.
   PubMed Web of Science ®Google Scholar
• Saw WY, Tantoso E, Begum H, Zhou L, Zou R, He C, Chan SL, Tan LW, Wong LP, Xu W, et al. Establishing multiple omics baselines for three Southeast Asian populations in the Singapore integrative omics study. Nat Commun. 2017;8(1):653. PMID:28935855. doi:10.1038/s41467-017-00413-x.
   PubMedGoogle Scholar
• Lv T, Shen L, Xu X, Yao Y, Mu P, Zhang H, Wan J, Wang Y, Guan R, Li X, et al. Patient-derived tumor organoids predict responses to irinotecan-based neoadjuvant chemoradiotherapy in patients with locally advanced rectal cancer. Int J Cancer. 2023;152(3):524–535. doi:10.1002/ijc.34302.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Garcia-Sanmartin J, Bobadilla M, Mirpuri E, Grifoll V, Perez-Clavijo M, Martinez A. Agaricus mushroom-enriched diets modulate the microbiota-gut-brain axis and reduce brain oxidative stress in mice. Antioxid (Basel). 2022;11(4). PMID:35453380. doi:10.3390/antiox11040695.
   PubMedGoogle Scholar
• Sookoian S, Salatino A, Castano GO, Landa MS, Fijalkowky C, Garaycoechea M, Pirola CJ. Intrahepatic bacterial metataxonomic signature in non-alcoholic fatty liver disease. Gut. 2020;69(8):1483–1491. PMID:31900291. doi:10.1136/gutjnl-2019-318811.
   PubMed Web of Science ®Google Scholar
• Constante M, Fragoso G, Calve A, Samba-Mondonga M, Santos MM. Dietary heme induces gut dysbiosis, aggravates colitis, and potentiates the development of adenomas in mice. Front Microbiol. 2017;8:1809. PMID:28983289. doi:10.3389/fmicb.2017.01809.
   PubMed Web of Science ®Google Scholar
• Seiwert N, Adam J, Steinberg P, Wirtz S, Schwerdtle T, Adams-Quack P, Hovelmeyer N, Kaina B, Foersch S, Fahrer J. Chronic intestinal inflammation drives colorectal tumor formation triggered by dietary heme iron in vivo. Arch Toxicol. 2021;95(7):2507–2522. PMID:33978766. doi:10.1007/s00204-021-03064-6.
   PubMed Web of Science ®Google Scholar
• Xiong Q, Zhao J, Tian C, Ma W, Miao L, Liang L, Zhang K, Du H. Regulation of a high-iron diet on lipid metabolism and gut microbiota in mice. Animals (Basel). 2022;12(16). PMID:36009656. doi:10.3390/ani12162063.
   Google Scholar
• Odenwald MA, Turner JR. The intestinal epithelial barrier: a therapeutic target? Nat Rev Gastroenterol Hepatol. 2017;14(1):9–21. PMID:27848962. doi:10.1038/nrgastro.2016.169.
   PubMed Web of Science ®Google Scholar
• Zhou A, Yuan Y, Yang M, Huang Y, Li X, Li S, Yang S, Tang B. Crosstalk between the gut microbiota and epithelial cells under physiological and infectious conditions. Front Cell Infect Microbiol. 2022;12:832672. PMID:35155283. doi:10.3389/fcimb.2022.832672.
   PubMed Web of Science ®Google Scholar
• Du XY, Liu X, Wang ZJ, Wang YY. SLPI promotes the gastric cancer growth and metastasis by regulating the expression of P53, Bcl-2 and Caspase-8. Eur Rev Med Pharmacol Sci. 2017;21:1495–1501. PMID:28429358.
   PubMed Web of Science ®Google Scholar
• Xia Y, Luo Q, Huang C, Shi L, Jahangir A, Pan T, Wei X, He J, Liu W, Shi R, et al. Ferric citrate-induced colonic mucosal damage associated with oxidative stress, inflammation responses, apoptosis, and the changes of gut microbial composition. Ecotoxicol Environ Saf. 2023;249:114364. PMID:36508806. doi:10.1016/j.ecoenv.2022.114364.
   PubMed Web of Science ®Google Scholar
• Wenhui Y, Zhongyu X, Kai C, Zhaopeng C, Jinteng L, Mengjun M, Zepeng S, Yunshu C, Peng W, Yanfeng W, et al. Variations in the gut microbiota in breast cancer occurrence and bone metastasis. Front Microbiol. 2022;13:894283. doi:10.3389/fmicb.2022.894283.
   PubMed Web of Science ®Google Scholar
• Finnicum CT, Rahal Z, Hassane M, Treekitkarnmongkol W, Sinjab A, Morris R, Liu Y, Tang EL, Viet S, Petersen JL, et al. Pathogenesis of tobacco-associated lung adenocarcinoma is closely coupled with changes in the gut and lung microbiomes. Int J Mol Sci. 2022;23(18):10930. PMID:36142843. doi:10.3390/ijms231810930.
   PubMed Web of Science ®Google Scholar
• Jafari M, Laraqui A, Baba W, Benmokhtar S, Zaitouni SE, Ali AA, Bounaim A, Moujahid M, Tanz R, Mahfoud T, et al. Prevalence and patterns of mutations in RAS/RAF/MEK/ERK/MAPK signaling pathway in colorectal cancer in North Africa. Bmc Cancer. 2022;22(1):1142. doi:10.1186/s12885-022-10235-w.
   PubMed Web of Science ®Google Scholar
• Huang C, Yi H, Zhou Y, Zhang Q, Yao X. Pan-cancer analysis reveals SH3TC2 as an oncogene for colorectal cancer and promotes tumorigenesis via the MAPK pathway. Cancers (Basel). 2022;14(15). PMID:35954399. doi:10.3390/cancers14153735.
   Web of Science ®Google Scholar
• Bai X, Wei H, Liu W, Coker OO, Gou H, Liu C, Zhao L, Li C, Zhou Y, Wang G, et al. Cigarette smoke promotes colorectal cancer through modulation of gut microbiota and related metabolites. Gut. 2022;71(12):2439–2450. PMID:35387878. doi:10.1136/gutjnl-2021-325021.
   PubMed Web of Science ®Google Scholar
• Togbe D, Schnyder-Candrian S, Schnyder B, Doz E, Noulin N, Janot L, Secher T, Gasse P, Lima C, Coelho FR, et al. Toll-like receptor and tumour necrosis factor dependent endotoxin-induced acute lung injury. Int J Exp Pathol. 2007;88(6):387–391. PMID:18039275. doi:10.1111/j.1365-2613.2007.00566.x.
   PubMed Web of Science ®Google Scholar
• Qi W, Liu J, Yu T, Huang S, Song R, Qiao Z. Ae1/Sbe1 maize-derived high amylose improves gut barrier function and ameliorates type II diabetes in high-fat diet-fed mice by increasing Akkermansia. Front Nutr. 2022;9:999020. PMID:36245499. doi:10.3389/fnut.2022.999020.
   PubMed Web of Science ®Google Scholar
• He Z, Wu J, Gong J, Ke J, Ding T, Zhao W, Cheng WM, Luo Z, He Q, Zeng W, et al. Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice. Microbio. 2021;9(1):228. PMID:34814945. doi:10.1186/s40168-021-01178-8.
   Google Scholar