How does carrageenan cause colitis? A review

Abraham, 1985, Chronic and subchronic effects of various forms of carrageenan in rats, Ecotoxicology and Environmental Safety, 10, 173, 10.1016/0147-6513(85)90063-6 Adnan, 2020, O-carboxymethylated chitosan; a promising tool with in-vivo anti-inflammatory and analgesic properties in albino rats, International Journal of Biological Macromolecules, 156, 531, 10.1016/j.ijbiomac.2020.04.038 Allen, 2019, Hyperadrenocorticism of calorie restriction contributes to its anti-inflammatory action in mice, Aging Cell, 18, 10.1111/acel.12944 Alqahtani, 2022, Anti-inflammatory potentials of β-ketoester derivatives of N-Ary succinimides: In vitro, in vivo, and molecular docking studies, Journal of Chemistry, 2022, 1, 10.1155/2022/8040322 Ananthakrishnan, 2018, Debate session: So what causes inflammatory bowel disease? It's all in the environment, Journal of Gastroenterology and Hepatology, 33, 24, 10.1111/jgh.14429 Anderson, 1967, Carrageenans and the proteolytic activity of human gastric secretion, Journal of Pharmacy And Pharmacology, 19, 720, 10.1111/j.2042-7158.1967.tb08023.x Azim, 2021, An in vivo evaluation of anti-inflammatory, analgesic and anti-pyretic activities of newly synthesized 1, 2, 4 triazole derivatives, BMC Complementary Medicine and Therapies, 21, 304, 10.1186/s12906-021-03485-x Bach Knudsen, 2018, Impact of diet-modulated butyrate production on intestinal barrier function and inflammation, Nutrients, 10, 1499, 10.3390/nu10101499 Bagues, 2017, Characterization of the nociceptive effect of carrageenan: Masseter versus gastrocnemius, Muscle & Nerve, 56, 804, 10.1002/mus.25538 Bancil, 2021, Food additive emulsifiers and their impact on gut microbiome, permeability, and inflammation: Mechanistic insights in inflammatory bowel disease, Journal of Crohns Colitis, 15, 1068, 10.1093/ecco-jcc/jjaa254 Baumgart, 2007, Inflammatory bowel disease: Clinical aspects and established and evolving therapies, The Lancet, 369, 1641, 10.1016/S0140-6736(07)60751-X Benard, 2010, Degraded carrageenan causing colitis in rats induces TNF secretion and ICAM-1 upregulation in monocytes through NF-kappaB activation, Public Library of Science One, 5 Bhattacharyya, 2008, Carrageenan induces cell cycle arrest in human intestinal epithelial cells in vitro, The Journal of Nutrition, 138, 469, 10.1093/jn/138.3.469 Bhattacharyya, 2007, Bcl10 mediates LPS-induced activation of NF-kappaB and IL-8 in human intestinal epithelial cells, American Journal of Physiology Gastrointestinal and Liver Physiology, 293, G429, 10.1152/ajpgi.00149.2007 Bhattacharyya, 2008, Carrageenan induces cell cycle arrest in human intestinal epithelial cells in vitro, The Journal of Nutrition, 138, 469, 10.1093/jn/138.3.469 Bhattacharyya, 2008, Carrageenan-induced NFkappaB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10, Biochimica et Biophysica Acta, 1780, 973, 10.1016/j.bbagen.2008.03.019 Bhattacharyya, 2008, Toll-like receptor 4 mediates induction of the Bcl10-NFkappaB-interleukin-8 inflammatory pathway by carrageenan in human intestinal epithelial cells, Journal of Biological Chemistry, 283, 10550, 10.1074/jbc.M708833200 Bhattacharyya, 2010, Tumor necrosis factor alpha-induced inflammation is increased but apoptosis is inhibited by common food additive carrageenan, Journal of Biological Chemistry, 285, 39511, 10.1074/jbc.M110.159681 Bhattacharyya, 2013, Carrageenan-induced colonic inflammation is reduced in Bcl10 null mice and increased in IL-10-deficient mice, Mediators of Inflammation, 2013, 1, 10.1155/2013/397642 Bhattacharyya, 2014, Common food additive carrageenan stimulates Wnt/beta-catenin signaling in colonic epithelium by inhibition of nucleoredoxin reduction, Nutrition and Cancer, 66, 117, 10.1080/01635581.2014.852228 Bhattacharyya, 2017, A randomized trial of the effects of the no-carrageenan diet on ulcerative colitis disease activity, Journal of Nutrition Health Aging, 4, 181, 10.3233/NHA-170023 Bian, 2022, A novel polysaccharide from Auricularia auricula alleviates thrombosis induced by carrageenan in mice, Molecules, 27, 4831, 10.3390/molecules27154831 Bian, 2019, Administration of Akkermansia muciniphila ameliorates dextran sulfate sodium-induced ulcerative colitis in mice, Frontiers in Microbiology, 10, 2259, 10.3389/fmicb.2019.02259 Bixler, 2017, The carrageenan controversy, Journal of Applied Phycology, 29, 2201, 10.1007/s10811-017-1132-4 Błaszak, 2018, Carrageenan as a functional additive in the production of cheese and cheese-like products, Acta Scientiarum Polonorum Technologia Alimentaria, 17, 107 Borsani, 2021, The role of carrageenan in inflammatory bowel diseases and allergic reactions: Where do we stand?, Nutrients, 13, 3402, 10.3390/nu13103402 Borthakur, 2007, Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells, American Journal of Physiology Gastrointestinal and Liver Physiology, 292, G829, 10.1152/ajpgi.00380.2006 Borthakur, 2007, Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells, American Journal of Physiology. Gastrointestinal and Liver Physiology, 292, G829, 10.1152/ajpgi.00380.2006 Borthakur, 2012, Prolongation of carrageenan-induced inflammation in human colonic epithelial cells by activation of an NFkappaB-BCL10 loop, Biochimica et Biophysica Acta, 1822, 1300, 10.1016/j.bbadis.2012.05.001 Bradley, 2017, Proteobacteria explain significant functional variability in the human gut microbiome, Microbiome, 5, 36, 10.1186/s40168-017-0244-z Brant, 2011, Update on the heritability of inflammatory bowel disease: The importance of twin studies, Inflammatory Bowel Diseases, 17, 1, 10.1002/ibd.21385 Chia, 2018, Deciphering the trophic interaction between Akkermansia muciniphila and the butyrogenic gut commensal Anaerostipes caccae using a metatranscriptomic approach, Antonie Van Leeuwenhoek, 111, 859, 10.1007/s10482-018-1040-x Chitsaz, 2023, Rubiadin exerts an acute and chronic anti-inflammatory effect in rodents, Brazilian Journal of Biology, 83, 10.1590/1519-6984.243775 Choi, 2012, Pro-inflammatory NF-kappaB and early growth response gene 1 regulate epithelial barrier disruption by food additive carrageenan in human intestinal epithelial cells, Toxicology Letters, 211, 289, 10.1016/j.toxlet.2012.04.012 Choi, 2018, Differential involvement of ipsilateral and contralateral spinal cord astrocyte D-serine in carrageenan-induced mirror-image pain: Role of sigma1 receptors and astrocyte gap junctions, British Journal of Pharmacology, 175, 558, 10.1111/bph.14109 Cohen, 2002, A critical review of the toxicological effects of carrageenan and processed eucheuma seaweed on the gastrointestinal tract, Critical Reviews in Toxicology, 32, 413, 10.1080/20024091064282 Costa, 2020, Chemical structure, anti-inflammatory and antinociceptive activities of a sulfated polysaccharide from Gracilaria intermedia algae, International Journal of Biological Macromolecules, 159, 966, 10.1016/j.ijbiomac.2020.05.166 Cui, 2019, Intestinal barrier function-non-alcoholic fatty liver disease interactions and possible role of gut microbiota, Journal of Agricultural and Food Chemistry, 67, 2754, 10.1021/acs.jafc.9b00080 Delahunty, 1987, Intestinal permeability changes in rodents a possible mechanism for degraded carrageenan induced colitis, Food and Chemical Toxicology, 25, 113, 10.1016/0278-6915(87)90143-8 Deng, 2019, Activated spinal astrocytes contribute to the later phase of carrageenan-induced prostatitis pain, Journal of Neuroinflammation, 16, 189, 10.1186/s12974-019-1584-3 Derrien, 2008, The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract, Applied and Environmental Microbiology, 74, 1646, 10.1128/AEM.01226-07 Earle, 2015, Quantitative imaging of gut microbiota spatial organization, Cell Host & Microbe, 18, 478, 10.1016/j.chom.2015.09.002 Earley, 2015, A preliminary study examining the binding capacity of Akkermansia muciniphila and Desulfovibrio spp., to colonic mucin in health and ulcerative colitis, Public Library of Science One, 10 Earley, 2019, The abundance of Akkermansia muciniphila and its relationship with sulphated colonic mucins in health and ulcerative colitis, Scientific Reports, 9, 15683, 10.1038/s41598-019-51878-3 Fahoum, 2017, Digestive fate of dietary carrageenan: Evidence of interference with digestive proteolysis and disruption of gut epithelial function, Molecular Nutrition Food Research, 61, 10.1002/mnfr.201600545 Fattori, 2019, The specialised pro-resolving lipid mediator maresin 1 reduces inflammatory pain with a long-lasting analgesic effect, British Journal of Pharmacology, 176, 1728, 10.1111/bph.14647 Fontenelle, 2018, Lectin obtained from the red seaweed Bryothamnion triquetrum: Secondary structure and anti-inflammatory activity in mice, International Journal of Biological Macromolecules, 112, 1122, 10.1016/j.ijbiomac.2018.02.058 de Freitas Pires, 2019, Lectin purified from Lonchocarpus campestris seeds inhibits inflammatory nociception, International Journal of Biological Macromolecules, 125, 53, 10.1016/j.ijbiomac.2018.11.233 Guilherme, 2022, Anti-inflammatory and analgesic evaluation of a phytochemical intercalated into layered double hydroxide, Pharmaceutics, 14, 934, 10.3390/pharmaceutics14050934 Guo, 2022, Physicochemical dynamic changes and differences of κ-carrageenan in different vehicles (aqueous and casein solution) during in vitro gastrointestinal digestion, Food Hydrocolloids, 129, 10.1016/j.foodhyd.2022.107553 Guo, 2020, Gut microbiota in ulcerative colitis: Insights on pathogenesis and treatment, Journal of Digestive Diseases, 21, 147, 10.1111/1751-2980.12849 Hansen, 2015, Immune responses to intestinal microbes in inflammatory bowel diseases, Current Allergy and Asthma Reports, 15, 61, 10.1007/s11882-015-0562-9 James, 2015, Abnormal fibre usage in UC in remission, Gut, 64, 562, 10.1136/gutjnl-2014-307198 Jiang, 2013, Kappa-carrageenan induces the disruption of intestinal epithelial Caco-2 monolayers by promoting the interaction between intestinal epithelial cells and immune cells, Molecular Medicine Reports, 8, 1635, 10.3892/mmr.2013.1726 Johansson, 2013, The gastrointestinal mucus system in health and disease, Nature Reviews Gastroenterology Hepatology, 10, 352, 10.1038/nrgastro.2013.35 Jostins, 2012, Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease, Nature, 491, 119, 10.1038/nature11582 Kang, 2013, Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis, Public Library of Science One, 8 Keightley, 2015, Gut feelings 2. Mind, mood and gut in inflammatory bowel disease: Approaches to psychiatric care, Australasian Psychiatry, 23, 407, 10.1177/1039856215590034 Khan, 2022, Suppression of NF-kappaB signaling by ECN in an arthritic model of inflammation, BMC Complementary Medicine and Therapies, 22, 158, 10.1186/s12906-022-03629-7 Kumar, 2020, A novel fibrinolytic enzyme from marine Pseudomonas aeruginosa KU1 and its rapid in vivo thrombolysis with little haemolysis, International Journal of Biological Macromolecules, 162, 470, 10.1016/j.ijbiomac.2020.06.178 Kurashima, 2017, Mucosal ecological network of epithelium and immune cells for gut homeostasis and tissue healing, Annual Review of Immunology, 35, 119, 10.1146/annurev-immunol-051116-052424 Lee, 2020, Carrageenans as broad-spectrum microbicides: Current status and challenges, Marine Drugs, 18, 435, 10.3390/md18090435 Li, 2015, Oral administration of Escin inhibits acute inflammation and reduces intestinal mucosal injury in animal models, Evidence-based Complementary and Alternative Medicine, 2015 Liu, 2021, Food-grade carrageenans and their implications in health and disease, Comprehensive Reviews in Food Science and Food Safety, 20, 3918, 10.1111/1541-4337.12790 Luissint, 2016, Inflammation and the intestinal barrier: Leukocyte-epithelial cell interactions, cell junction remodeling, and mucosal repair, Gastroenterology, 151, 616, 10.1053/j.gastro.2016.07.008 Martino, 2017, The role of carrageenan and carboxymethylcellulose in the development of intestinal inflammation, Frontiers in Pediatrics, 5, 10.3389/fped.2017.00096 Mazzarella, 2015, Effector and suppressor T cells in celiac disease, World Journal of Gastroenterology, 21, 7349, 10.3748/wjg.v21.i24.7349 McKim, 2014, Food additive carrageenan: Part I: A critical review of carrageenan in vitro studies, potential pitfalls, and implications for human health and safety, Critical Reviews in Toxicology, 44, 211, 10.3109/10408444.2013.861797 McKim, 2016, Effects of carrageenan on cell permeability, cytotoxicity, and cytokine gene expression in human intestinal and hepatic cell lines, Food and Chemical Toxicology, 96, 1, 10.1016/j.fct.2016.07.006 Mi, 2020, Native kappa-carrageenan induced-colitis is related to host intestinal microecology, International Journal of Biological Macromolecules, 147, 284, 10.1016/j.ijbiomac.2020.01.072 Michel, 1996, Digestive fates of soluble polysaccharides from marine macroalgae involvement of the colonic microflora and physiological consequences for the hos, Journal of Applied Bacteriology, 80, 349, 10.1111/j.1365-2672.1996.tb03230.x Mitra, 2022, Pharmacological potential of avicennia alba leaf extract: An experimental analysis focusing on antidiabetic, anti-inflammatory, analgesic, and antidiarrheal activity, BioMed Research International, 2022, 10.1155/2022/7624189 Munyaka, 2016, Carrageenan gum and adherent invasive Escherichia coli in a piglet model of inflammatory bowel disease: Impact on intestinal mucosa-associated microbiota, Frontiers in Microbiology, 7, 462, 10.3389/fmicb.2016.00462 Nguyen, 2020, Antipyretic, anti-inflammatory and analgesic activities of Periplaneta americana extract and underlying mechanisms, Biomedicine & Pharmacotherapy, 123, 10.1016/j.biopha.2019.109753 Nishida, 2012, The membrane-bound mucin Muc1 regulates T helper 17-cell responses and colitis in mice, Gastroenterology, 142 Okumura, 2017, Roles of intestinal epithelial cells in the maintenance of gut homeostasis, Experimental and Molecular Medicine, 49, 10.1038/emm.2017.20 Ottman, 2017, Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle, Applied and Environmental Microbiology, 83, 10.1128/AEM.01014-17 Ottman, 2017, Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function, Public Library of Science One, 12 Pei, 2019, Role of colonic microbiota in the pathogenesis of ulcerative colitis, BMC Gastroenterology, 19, 10, 10.1186/s12876-019-0930-3 Permpoon, 2017, Ethnic variations in ulcerative colitis: Experience of an international hospital in Thailand, Clinical Gastroenterology and Hepatology, 15, 10.1016/j.cgh.2016.09.044 Ramos, 2019, Mechanisms of disease: Inflammatory bowel diseases, Mayo Clinic Proceedings, 94, 155, 10.1016/j.mayocp.2018.09.013 Reunanen, 2015, Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer, Applied and Environmental Microbiology, 81, 3655, 10.1128/AEM.04050-14 Shang, 2017, Carrageenan-induced colitis is associated with decreased population of anti-inflammatory bacterium, Akkermansia muciniphila, in the gut microbiota of C57BL/6J mice, Toxicology Letters, 279, 87, 10.1016/j.toxlet.2017.07.904 Shen, 2018, Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation, World Journal of Gastroenterology, 24, 5, 10.3748/wjg.v24.i1.5 Shrimali, 2021, Alpha-ketoglutarate inhibits thrombosis and inflammation by prolyl hydroxylase-2 mediated inactivation of phospho-akt, eBioMedicine, 73, 10.1016/j.ebiom.2021.103672 Silva, 2021, Tagitinin F has anti-inflammatory, anti-nociceptive and anti-matrix metalloproteinase properties: An in silico, in vitro and in vivo study, Pharmacological Research, 164, 10.1016/j.phrs.2020.105303 Singh, 2016, Food additive P-80 impacts mouse gut microbiota promoting intestinal inflammation, obesity and liver dysfunction, Diagnostic Microbiology and Infectious Disease, 4, 1 Souza, 2016, Immunopathogenesis of IBD: Current state of the art, Nature Reviews. Gastroenterology & Hepatology, 13, 13, 10.1038/nrgastro.2015.186 Sun, 2019, In vitro fermentation of κ-carrageenan oligosaccharides by human gut microbiota and its inflammatory effect on HT29 cells, Journal of Functional Foods, 59, 80, 10.1016/j.jff.2019.05.036 Tkachenko, 2020, Experimental evaluation of the impact of gadolinium orthovanadate GdVO4:Eu3+ nanoparticles on the carrageenan-induced intestinal inflammation, Acta Medica (Hradec Králové), 63, 18 Tobacman, 1997, Filament disassembly and loss of mammary myoepithelial cells after exposure to lambda-carrageenan, Cancer Research Tobacman, 2001, Review of harmful gastrointestinal effects of carrageenan in animal experiments, Environmental Health Perspectives, 109, 983, 10.1289/ehp.01109983 Tsuji, 2003, Suppression of allergic reaction by lambda-carrageenan toll-like receptor 4MyD88 dependent and independent modulation of immunity, Clinical and Experimental Allergy, 33, 249, 10.1046/j.1365-2222.2003.01575.x Wang, 2020, The variable oligomeric state of Amuc_1100 from Akkermansia muciniphila, Journal of Structural Biology, 212, 10.1016/j.jsb.2020.107593 Wang, 2016, Research advance in intestinal mucosal barrier and pathogenesis of Crohn's disease, Gastroenterology Research and Practice, 2016, 1 Wang, 2021, Effect of κ-carrageenan on glucolipid metabolism and gut microbiota in high-fat diet-fed mice, Journal of Functional Foods, 86, 10.1016/j.jff.2021.104707 Watson, 2007, Public health and carrageenan regulation: A review and analysis, Journal of Applied Phycology, 20, 505, 10.1007/s10811-007-9252-x Watt, 1969, Ulcerative colitis in the Guinea-pig caused by seaweed extract, Journal of Pharmacy and Pharmacology, 21, 187, 10.1111/j.2042-7158.1969.tb08372.x Wei, 2016, Enhanced effect of kappa-carrageenan on TNBS-induced inflammation in mice, International Immunopharmacology, 39, 218, 10.1016/j.intimp.2016.07.031 Weiner, 2014, Food additive carrageenan: Part II: A critical review of carrageenan in vivo safety studies, Critical Reviews in Toxicology, 44, 244, 10.3109/10408444.2013.861798 Weiner, 2015, An infant formula toxicity and toxicokinetic feeding study on carrageenan in preweaning piglets with special attention to the immune system and gastrointestinal tract, Food and Chemical Toxicology, 77, 120, 10.1016/j.fct.2014.12.022 Willemsen, 2005, Abrogation of IFN-gamma mediated epithelial barrier disruption by serine protease inhibition, Clinical and Experimental Immunology, 142, 275, 10.1111/j.1365-2249.2005.02906.x Wu, 2016, Synergistic effect of kappa-carrageenan on oxazolone-induced inflammation in BALB/c mice, BMC Gastroenterology, 16, 41, 10.1186/s12876-016-0459-7 Wu, 2017, Kappa-carrageenan enhances lipopolysaccharide-induced interleukin-8 secretion by stimulating the Bcl10-NF-kappaB pathway in HT-29 cells and aggravates C. freundii-induced inflammation in mice, Mediators of Inflammation, 2017, 1, 10.1155/2017/6598540 Wu, 2021, Lambda-carrageenan exacerbates Citrobacter rodentium-induced infectious colitis in mice by targeting gut microbiota and intestinal barrier integrity, Pharmacological Research, 174, 10.1016/j.phrs.2021.105940 Wu, 2022, Dietary kappa-carrageenan facilitates gut microbiota-mediated intestinal inflammation, Carbohydrate Polymers, 277, 10.1016/j.carbpol.2021.118830 Wu, 2019, The role of autophagy in maintaining intestinal mucosal barrier, Journal of Cellular Physiology, 234, 19406, 10.1002/jcp.28722 Xu, 2016, Effect of tight junction protein of intestinal epithelium and permeability of colonic mucosa in pathogenesis of injured colonic barrier during chronic recovery stage of rats with inflammatory bowel disease, Asian Pacific Journal of Tropical Medicine, 9, 148, 10.1016/j.apjtm.2016.01.001 Yamada, 2016, Role of regulatory T cell in the pathogenesis of inflammatory bowel disease, World Journal of Gastroenterology, 22, 2195, 10.3748/wjg.v22.i7.2195 Yang, 2012, Exposure to common food additive carrageenan leads to reduced sulfatase activity and increase in sulfated glycosaminoglycans in human epithelial cells, Biochimie, 94, 1309, 10.1016/j.biochi.2012.02.031 Yang, 2019, TLR9 limits enteric antimicrobial responses and promotes microbiota-based colonisation resistance during Citrobacter rodentium infection, Cellular Microbiology, 21, 10.1111/cmi.13026 Yao, 2022, Advances in anti-cancer effects and underlying mechanisms of marine algae polysaccharides, International Journal of Biological Macromolecules, 221, 472, 10.1016/j.ijbiomac.2022.09.055 Yin, 2021, Carrageenan oligosaccharides and associated carrageenan-degrading bacteria induce intestinal inflammation in germ-free mice, Journal of Genetics and Genomics, 48, 815, 10.1016/j.jgg.2021.08.001 Yu, 2021, Layered dissolving microneedles as a need-based delivery system to simultaneously alleviate skin and joint lesions in psoriatic arthritis, Acta Pharmaceutica Sinica B, 11, 505, 10.1016/j.apsb.2020.08.008 Yu, 2018, Berberrubine attenuates mucosal lesions and inflammation in dextran sodium sulfate-induced colitis in mice, Public Library of Science One, 13 Zhai, 2019, Strain-specific anti-inflammatory properties of two Akkermansia muciniphila strains on chronic colitis in mice, Frontiers in Cellular and Infection Microbiology, 9, 239, 10.3389/fcimb.2019.00239 Zhao, 2015, Moxibustion and acupuncture ameliorate Crohn's disease by regulating the balance between Th17 and Treg cells in the intestinal mucosa, Evidence-based Complementary and Alternative Medicine, 2015, 10.1155/2015/938054