Anti-Inflammatory Effects of Algae-Derived Biomolecules in Gut Health: A Review
Abstract
1. Introduction
2. Materials and Methods
3. IBD Pathophysiology
3.1. Characterization of IBD Patients’ Intestinal Mucosa
3.2. Innate Immune System Activation
3.3. Neutrophils in IBD Pathogenesis
3.4. Oxidative Stress in IBD Pathogenesis
3.5. Macrophages in IBD Pathogenesis
3.6. Current Treatment
4. Potential of Algae-Derived Biomolecules in IBD Treatment
4.1. Natural Compounds in IBD Studies
4.2. Anti-Inflammatory Activity of Chlorophyta (Green Algae) Extracts
4.3. Anti-Inflammatory Activity of Phaeophyta (Brown Algae) Extracts
4.4. Anti-Inflammatory Activity of Rhodophyta (Red Algae) Extracts
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Loftus, E.V. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology 2004, 126, 1504–1517. [Google Scholar] [CrossRef] [PubMed]
- Eisenstein, M. Ulcerative colitis: Towards remission. Nature 2018, 563, S33. [Google Scholar] [CrossRef] [PubMed]
- Molodecky, N.A.; Soon, I.S.; Rabi, D.M.; Ghali, W.A.; Ferris, M.; Chernoff, G.; Benchimol, E.I.; Panaccione, R.; Ghosh, S.; Barkema, H.W.; et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012, 142, 46–54.e42, quiz e30. [Google Scholar] [CrossRef]
- Baumgart, D.C.; Sandborn, W.J. Crohn’s disease. Lancet 2012, 380, 1590–1605. [Google Scholar] [CrossRef] [PubMed]
- Argollo, M.; Gilardi, D.; Peyrin-Biroulet, C.; Chabot, J.-F.; Peyrin-Biroulet, L.; Danese, S. Comorbidities in inflammatory bowel disease: A call for action. Lancet Gastroenterol. Hepatol. 2019, 4, 643–654. [Google Scholar] [CrossRef] [PubMed]
- Kaplan, G.G.; Windsor, J.W. The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 56–66. [Google Scholar] [CrossRef] [PubMed]
- Danese, S. Immune and nonimmune components orchestrate the pathogenesis of inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300, G716–G722. [Google Scholar] [CrossRef]
- Vebr, M.; Pomahačová, R.; Sýkora, J.; Schwarz, J. A Narrative Review of Cytokine Networks: Pathophysiological and Therapeutic Implications for Inflammatory Bowel Disease Pathogenesis. Biomedicines 2023, 11, 3229. [Google Scholar] [CrossRef] [PubMed]
- Genaro, L.M.; Gomes, L.E.M.; de Freitas Franceschini, A.P.M.; Ceccato, H.D.; de Jesus, R.N.; Lima, A.P.; Nagasako, C.K.; Fagundes, J.J.; Ayrizono, M.D.L.S.; Leal, R.F. Anti-TNF therapy and immunogenicity in inflammatory bowel diseases: A translational approach. Am. J. Transl. Res. 2021, 13, 13916–13930. [Google Scholar]
- Alshehri, D.; Saadah, O.; Mosli, M.; Edris, S.; Alhindi, R.; Bahieldin, A. Dysbiosis of gut microbiota in inflammatory bowel disease: Current therapies and potential for microbiota-modulating therapeutic approaches. Bosn. J. Basic Med. Sci. 2021, 21, 270–283. [Google Scholar] [CrossRef]
- Khor, B.; Gardet, A.; Xavier, R.J. Genetics and pathogenesis of inflammatory bowel disease. Nature 2011, 474, 307–317. [Google Scholar] [CrossRef]
- Quévrain, E.; Maubert, M.A.; Michon, C.; Chain, F.; Marquant, R.; Tailhades, J.; Miquel, S.; Carlier, L.; Bermúdez-Humarán, L.G.; Pigneur, B.; et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut 2016, 65, 415–425. [Google Scholar] [CrossRef]
- Taylor, C.T.; Colgan, S.P. Regulation of immunity and inflammation by hypoxia in immunological niches. Nat. Rev. Immunol. 2017, 17, 774–785. [Google Scholar] [CrossRef]
- Sahoo, D.K.; Heilmann, R.M.; Paital, B.; Patel, A.; Yadav, V.K.; Wong, D.; Jergens, A.E. Oxidative stress, hormones, and effects of natural antioxidants on intestinal inflammation in inflammatory bowel disease. Front. Endocrinol. 2023, 14, 1217165. [Google Scholar] [CrossRef]
- Park, J.; Cheon, J.H. Updates on conventional therapies for inflammatory bowel diseases: 5-aminosalicylates, corticosteroids, immunomodulators, and anti-TNF-α. Korean J. Intern. Med. 2022, 37, 895–905. [Google Scholar] [CrossRef]
- Ramos-Romero, S.; Torrella, J.R.; Pagès, T.; Viscor, G.; Torres, J.L. Edible Microalgae and Their Bioactive Compounds in the Prevention and Treatment of Metabolic Alterations. Nutrients 2021, 13, 563. [Google Scholar] [CrossRef] [PubMed]
- Uzair, B.; Liaqat, A.; Iqbal, H.; Menaa, B.; Razzaq, A.; Thiripuranathar, G.; Fatima Rana, N.; Menaa, F. Green and Cost-Effective Synthesis of Metallic Nanoparticles by Algae: Safe Methods for Translational Medicine. Bioengineering 2020, 7, 129. [Google Scholar] [CrossRef]
- Menaa, F.; Wijesinghe, U.; Thiripuranathar, G.; Althobaiti, N.A.; Albalawi, A.E.; Khan, B.A.; Menaa, B. Marine Algae-Derived Bioactive Compounds: A New Wave of Nanodrugs? Mar. Drugs 2021, 19, 484. [Google Scholar] [CrossRef]
- Velankanni, P.; Go, S.-H.; Jin, J.B.; Park, J.-S.; Park, S.; Lee, S.-B.; Kwon, H.-K.; Pan, C.-H.; Cha, K.H.; Lee, C.-G. Chlorella vulgaris Modulates Gut Microbiota and Induces Regulatory T Cells to Alleviate Colitis in Mice. Nutrients 2023, 15, 3293. [Google Scholar] [CrossRef] [PubMed]
- Ardizzone, A.; Filippone, A.; Mannino, D.; Scuderi, S.A.; Casili, G.; Lanza, M.; Cucinotta, L.; Campolo, M.; Esposito, E. Ulva pertusa, a Marine Green Alga, Attenuates DNBS-Induced Colitis Damage via NF-κB/Nrf2/SIRT1 Signaling Pathways. J. Clin. Med. 2022, 11, 4301. [Google Scholar] [CrossRef] [PubMed]
- Ardizzone, A.; Mannino, D.; Capra, A.P.; Repici, A.; Filippone, A.; Esposito, E.; Campolo, M. New Insights into the Mechanism of Ulva pertusa on Colitis in Mice: Modulation of the Pain and Immune System. Mar. Drugs 2023, 21, 298. [Google Scholar] [CrossRef]
- Bagalagel, A.; Diri, R.; Noor, A.; Almasri, D.; Bakhsh, H.T.; Kutbi, H.I.; Al-Gayyar, M.M.H. Curative effects of fucoidan on acetic acid induced ulcerative colitis in rats via modulating aryl hydrocarbon receptor and phosphodiesterase-4. BMC Complement. Med. Ther. 2022, 22, 196. [Google Scholar] [CrossRef] [PubMed]
- Nemoto, M.; Kuda, T.; Eda, M.; Yamakawa, H.; Takahashi, H.; Kimura, B. Protective Effects of Mekabu Aqueous Solution Fermented by Lactobacillus plantarum Sanriku-SU7 on Human Enterocyte-Like HT-29-luc Cells and DSS-Induced Murine IBD Model. Probiotics Antimicrob. Proteins 2017, 9, 48–55. [Google Scholar] [CrossRef]
- Ahmad, T.; Ishaq, M.; Karpiniec, S.; Park, A.; Stringer, D.; Singh, N.; Ratanpaul, V.; Wolfswinkel, K.; Fitton, H.; Caruso, V.; et al. Oral Macrocystis pyrifera Fucoidan Administration Exhibits Anti-Inflammatory and Antioxidant Properties and Improves DSS-Induced Colitis in C57BL/6J Mice. Pharmaceutics 2022, 14, 2383. [Google Scholar] [CrossRef]
- Rehman, S.; Gora, A.H.; Abdelhafiz, Y.; Dias, J.; Pierre, R.; Meynen, K.; Fernandes, J.M.O.; Sørensen, M.; Brugman, S.; Kiron, V. Potential of algae-derived alginate oligosaccharides and β-glucan to counter inflammation in adult zebrafish intestine. Front. Immunol. 2023, 14, 1183701. [Google Scholar] [CrossRef]
- Lucena, A.M.M.; Souza, C.R.M.; Jales, J.T.; Guedes, P.M.M.; de Miranda, G.E.C.; de Moura, A.M.A.; Araújo-Júnior, J.X.; Nascimento, G.J.; Scortecci, K.C.; Santos, B.V.O.; et al. The Bisindole Alkaloid Caulerpin, from Seaweeds of the Genus Caulerpa, Attenuated Colon Damage in Murine Colitis Model. Mar. Drugs 2018, 16, 318. [Google Scholar] [CrossRef]
- Liao, M.; Wei, S.; Hu, X.; Liu, J.; Wang, J. Protective Effect and Mechanisms of Eckol on Chronic Ulcerative Colitis Induced by Dextran Sulfate Sodium in Mice. Mar. Drugs 2023, 21, 376. [Google Scholar] [CrossRef]
- Zhu, X.; Sun, Y.; Zhang, Y.; Su, X.; Luo, C.; Alarifi, S.; Yang, H. Dieckol alleviates dextran sulfate sodium-induced colitis via inhibition of inflammatory pathway and activation of Nrf2/HO-1 signaling pathway. Environ. Toxicol. 2021, 36, 782–788. [Google Scholar] [CrossRef]
- Joung, E.-J.; Cao, L.; Gwon, W.-G.; Kwon, M.-S.; Lim, K.T.; Kim, H.-R. Meroterpenoid-Rich Ethanoic Extract of Sargassum macrocarpum Ameliorates Dextran Sulfate Sodium-Induced Colitis in Mice. Foods 2022, 11, 329. [Google Scholar] [CrossRef]
- Yamada, S.; Koyama, T.; Noguchi, H.; Ueda, Y.; Kitsuyama, R.; Shimizu, H.; Tanimoto, A.; Wang, K.-Y.; Nawata, A.; Nakayama, T.; et al. Marine Hydroquinone Zonarol Prevents Inflammation and Apoptosis in Dextran Sulfate Sodium-Induced Mice Ulcerative Colitis. PLoS ONE 2014, 9, e113509. [Google Scholar] [CrossRef]
- Kim, N.-H.; Lee, S.M.; Kim, Y.N.; Jeon, Y.-J.; Heo, J.-D.; Jeong, E.J.; Rho, J.-R. Standardized Fraction of Turbinaria ornata Alleviates Dextran Sulfate Sodium-Induced Chronic Colitis in C57BL/6 Mice via Upregulation of FOXP3+ Regulatory T Cells. Biomolecules 2020, 10, 1463. [Google Scholar] [CrossRef]
- Kim, J.; Choi, J.H.; Ko, G.; Jo, H.; Oh, T.; Ahn, B.; Unno, T. Anti-Inflammatory Properties and Gut Microbiota Modulation of Porphyra tenera Extracts in Dextran Sodium Sulfate-Induced Colitis in Mice. Antioxidants 2020, 9, 988. [Google Scholar] [CrossRef]
- da Costa, E.; Melo, T.; Reis, M.; Domingues, P.; Calado, R.; Abreu, M.H.; Domingues, M.R. Polar Lipids Composition, Antioxidant and Anti-Inflammatory Activities of the Atlantic Red Seaweed Grateloupia turuturu. Mar. Drugs 2021, 19, 414. [Google Scholar] [CrossRef]
- Schroeder, B.O.; Birchenough, G.M.H.; Ståhlman, M.; Arike, L.; Johansson, M.E.V.; Hansson, G.C.; Bäckhed, F. Bifidobacteria or Fiber Protects against Diet-Induced Microbiota-Mediated Colonic Mucus Deterioration. Cell Host Microbe 2018, 23, 27–40.e7. [Google Scholar] [CrossRef]
- Ananthakrishnan, A.N.; Bernstein, C.N.; Iliopoulos, D.; Macpherson, A.; Neurath, M.F.; Ali, R.A.R.; Vavricka, S.R.; Fiocchi, C. Environmental triggers in IBD: A review of progress and evidence. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 39–49. [Google Scholar] [CrossRef]
- Ghilas, S.; O’Keefe, R.; Mielke, L.A.; Raghu, D.; Buchert, M.; Ernst, M. Crosstalk between epithelium, myeloid and innate lymphoid cells during gut homeostasis and disease. Front. Immunol. 2022, 13, 944982. [Google Scholar] [CrossRef] [PubMed]
- Saez, A.; Herrero-Fernandez, B.; Gomez-Bris, R.; Sánchez-Martinez, H.; Gonzalez-Granado, J.M. Pathophysiology of Inflammatory Bowel Disease: Innate Immune System. Int. J. Mol. Sci. 2023, 24, 1526. [Google Scholar] [CrossRef]
- Kinchen, J.; Chen, H.H.; Parikh, K.; Antanaviciute, A.; Jagielowicz, M.; Fawkner-Corbett, D.; Ashley, N.; Cubitt, L.; Mellado-Gomez, E.; Attar, M.; et al. Structural Remodeling of the Human Colonic Mesenchyme in Inflammatory Bowel Disease. Cell 2018, 175, 372–386.e17. [Google Scholar] [CrossRef]
- Bassler, K.; Schulte-Schrepping, J.; Warnat-Herresthal, S.; Aschenbrenner, A.C.; Schultze, J.L. The Myeloid Cell Compartment—Cell by Cell. Annu. Rev. Immunol. 2019, 37, 269–293. [Google Scholar] [CrossRef]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.-C. NF-κB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef]
- Chen, F.; Liu, Y.; Shi, Y.; Zhang, J.; Liu, X.; Liu, Z.; Lv, J.; Leng, Y. The emerging role of neutrophilic extracellular traps in intestinal disease. Gut Pathog. 2022, 14, 27. [Google Scholar] [CrossRef]
- Dinallo, V.; Marafini, I.; Di Fusco, D.; Laudisi, F.; Franzè, E.; Di Grazia, A.; Figliuzzi, M.M.; Caprioli, F.; Stolfi, C.; Monteleone, I.; et al. Neutrophil Extracellular Traps Sustain Inflammatory Signals in Ulcerative Colitis. J. Crohns Colitis 2019, 13, 772–784. [Google Scholar] [CrossRef]
- Kałużna, A.; Olczyk, P.; Komosińska-Vassev, K. The Role of Innate and Adaptive Immune Cells in the Pathogenesis and Development of the Inflammatory Response in Ulcerative Colitis. J. Clin. Med. 2022, 11, 400. [Google Scholar] [CrossRef]
- Hansberry, D.R.; Shah, K.; Agarwal, P.; Agarwal, N. Fecal Myeloperoxidase as a Biomarker for Inflammatory Bowel Disease. Cureus 2017, 9, e1004. [Google Scholar] [CrossRef]
- Maronek, M.; Gromova, B.; Liptak, R.; Konecna, B.; Pastorek, M.; Cechova, B.; Harsanyova, M.; Budis, J.; Smolak, D.; Radvanszky, J.; et al. Extracellular DNA Correlates with Intestinal Inflammation in Chemically Induced Colitis in Mice. Cells 2021, 10, 81. [Google Scholar] [CrossRef]
- Wéra, O.; Lancellotti, P.; Oury, C. The Dual Role of Neutrophils in Inflammatory Bowel Diseases. J. Clin. Med. 2016, 5, 118. [Google Scholar] [CrossRef]
- Tian, T.; Wang, Z.; Zhang, J. Pathomechanisms of Oxidative Stress in Inflammatory Bowel Disease and Potential Antioxidant Therapies. Oxid. Med. Cell. Longev. 2017, 2017, 4535194. [Google Scholar] [CrossRef]
- Colgan, S.P.; Taylor, C.T. Hypoxia: An alarm signal during intestinal inflammation. Nat. Rev. Gastroenterol. Hepatol. 2010, 7, 281–287. [Google Scholar] [CrossRef]
- Moret-Tatay, I.; Iborra, M.; Cerrillo, E.; Tortosa, L.; Nos, P.; Beltrán, B. Possible Biomarkers in Blood for Crohn’s Disease: Oxidative Stress and MicroRNAs—Current Evidences and Further Aspects to Unravel. Oxid. Med. Cell. Longev. 2016, 2016, 2325162. [Google Scholar] [CrossRef] [PubMed]
- Balmus, I.M.; Ciobica, A.; Trifan, A.; Stanciu, C. The Implications of Oxidative Stress and Antioxidant Therapies in Inflammatory Bowel Disease: Clinical Aspects and Animal Models. Saudi J. Gastroenterol. 2016, 22, 3. [Google Scholar] [CrossRef]
- Rugtveit, J.; Nilsen, E.M.; Bakka, A.; Carlsen, H.; Brandtzaeg, P.; Scott, H. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastroenterology 1997, 112, 1493–1505. [Google Scholar] [CrossRef]
- Mosser, D.M.; Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8, 958–969. [Google Scholar] [CrossRef]
- El Sayed, S.; Patik, I.; Redhu, N.S.; Glickman, J.N.; Karagiannis, K.; El Naenaeey, E.S.Y.; Elmowalid, G.A.; Abd El Wahab, A.M.; Snapper, S.B.; Horwitz, B.H. CCR2 promotes monocyte recruitment and intestinal inflammation in mice lacking the interleukin-10 receptor. Sci. Rep. 2022, 12, 452. [Google Scholar] [CrossRef]
- Zigmond, E.; Varol, C.; Farache, J.; Elmaliah, E.; Satpathy, A.T.; Friedlander, G.; Mack, M.; Shpigel, N.; Boneca, I.G.; Murphy, K.M.; et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 2012, 37, 1076–1090. [Google Scholar] [CrossRef]
- Zwicker, S.; Martinez, G.L.; Bosma, M.; Gerling, M.; Clark, R.; Majster, M.; Söderman, J.; Almer, S.; Boström, E.A. Interleukin 34: A new modulator of human and experimental inflammatory bowel disease. Clin. Sci. 2015, 129, 281–290. [Google Scholar] [CrossRef]
- Franzè, E.; Dinallo, V.; Laudisi, F.; Di Grazia, A.; Di Fusco, D.; Colantoni, A.; Ortenzi, A.; Giuffrida, P.; Di Carlo, S.; Sica, G.S.; et al. Interleukin-34 Stimulates Gut Fibroblasts to Produce Collagen Synthesis. J. Crohns Colitis 2020, 14, 1436–1445. [Google Scholar] [CrossRef]
- Wang, Y.; Huang, B.; Jin, T.; Ocansey, D.K.W.; Jiang, J.; Mao, F. Intestinal Fibrosis in Inflammatory Bowel Disease and the Prospects of Mesenchymal Stem Cell Therapy. Front. Immunol. 2022, 13, 835005. [Google Scholar] [CrossRef]
- Hinz, B.; Lagares, D. Evasion of apoptosis by myofibroblasts: A hallmark of fibrotic diseases. Nat. Rev. Rheumatol. 2020, 16, 11–31. [Google Scholar] [CrossRef]
- Zegarra Ruiz, D.F.; Kim, D.V.; Norwood, K.; Saldana-Morales, F.B.; Kim, M.; Ng, C.; Callaghan, R.; Uddin, M.; Chang, L.-C.; Longman, R.S.; et al. Microbiota manipulation to increase macrophage IL-10 improves colitis and limits colitis-associated colorectal cancer. Gut Microbes 2022, 14, 2119054. [Google Scholar] [CrossRef]
- Bryant, R.V.; Brain, O.; Travis, S.P.L. Conventional drug therapy for inflammatory bowel disease. Scand. J. Gastroenterol. 2015, 50, 90–112. [Google Scholar] [CrossRef]
- Louis, E.; Paridaens, K.; Al Awadhi, S.; Begun, J.; Cheon, J.H.; Dignass, A.U.; Magro, F.; Márquez, J.R.; Moschen, A.R.; Narula, N.; et al. Modelling the benefits of an optimised treatment strategy for 5-ASA in mild-to-moderate ulcerative colitis. BMJ Open Gastroenterol. 2022, 9, e000853. [Google Scholar] [CrossRef]
- Wild, G.E.; Waschke, K.A.; Bitton, A.; Thomson, A.B.R. The mechanisms of prednisone inhibition of inflammation in Crohn’s disease involve changes in intestinal permeability, mucosal TNFalpha production and nuclear factor kappa B expression. Aliment. Pharmacol. Ther. 2003, 18, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Waljee, A.K.; Wiitala, W.L.; Govani, S.; Stidham, R.; Saini, S.; Hou, J.; Feagins, L.A.; Khan, N.; Good, C.B.; Vijan, S.; et al. Corticosteroid Use and Complications in a US Inflammatory Bowel Disease Cohort. PLoS ONE 2016, 11, e0158017. [Google Scholar] [CrossRef] [PubMed]
- Buchman, A.L. Side effects of corticosteroid therapy. J. Clin. Gastroenterol. 2001, 33, 289–294. [Google Scholar] [CrossRef] [PubMed]
- Velayos, F.; Mahadevan, U. Management of Steroid-Dependent Ulcerative Colitis: Immunomodulatory Agents, Biologics, or Surgery? Clin. Gastroenterol. Hepatol. 2007, 5, 668–671. [Google Scholar] [CrossRef]
- Lees, C.W.; Maan, A.K.; Hansoti, B.; Satsangi, J.; Arnott, I.D.R. Tolerability and safety of mercaptopurine in azathioprine-intolerant patients with inflammatory bowel disease. Aliment. Pharmacol. Ther. 2008, 27, 220–227. [Google Scholar] [CrossRef] [PubMed]
- Stournaras, E.; Qian, W.; Pappas, A.; Hong, Y.Y.; Shawky, R.; Raine, T.; Parkes, M. Thiopurine monotherapy is effective in ulcerative colitis but significantly less so in Crohn’s disease: Long-term outcomes for 11 928 patients in the UK inflammatory bowel disease bioresource. Gut 2021, 70, 677–686. [Google Scholar] [CrossRef] [PubMed]
- Lamb, C.A.; Kennedy, N.A.; Raine, T.; Hendy, P.A.; Smith, P.J.; Limdi, J.K.; Hayee, B.; Lomer, M.C.E.; Parkes, G.C.; Selinger, C.; et al. British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 2019, 68, s1–s106. [Google Scholar] [CrossRef] [PubMed]
- Xu, Z.; Davis, H.M.; Zhou, H. Clinical impact of concomitant immunomodulators on biologic therapy: Pharmacokinetics, immunogenicity, efficacy and safety. J. Clin. Pharmacol. 2015, 55, S60–S74. [Google Scholar] [CrossRef] [PubMed]
- Vulliemoz, M.; Brand, S.; Juillerat, P.; Mottet, C.; Ben-Horin, S.; Michetti, P.; on behalf of Swiss IBDnet, an official working group of the Swiss Society of Gastroenterology. TNF-Alpha Blockers in Inflammatory Bowel Diseases: Practical Recommendations and a User’s Guide: An Update. Digestion 2020, 101, 16–26. [Google Scholar] [CrossRef]
- Annese, V.; Beaugerie, L.; Egan, L.; Biancone, L.; Bolling, C.; Brandts, C.; Dierickx, D.; Dummer, R.; Fiorino, G.; Gornet, J.M.; et al. European Evidence-based Consensus: Inflammatory Bowel Disease and Malignancies. J. Crohns Colitis 2015, 9, 945–965. [Google Scholar] [CrossRef] [PubMed]
- Murdaca, G.; Spanò, F.; Contatore, M.; Guastalla, A.; Penza, E.; Magnani, O.; Puppo, F. Infection risk associated with anti-TNF-α agents: A review. Expert Opin. Drug Saf. 2015, 14, 571–582. [Google Scholar] [CrossRef] [PubMed]
- Udenigwe, C.C.; Aluko, R.E. Food protein-derived bioactive peptides: Production, processing, and potential health benefits. J. Food Sci. 2012, 77, R11–R24. [Google Scholar] [CrossRef]
- Newman, D.J.; Cragg, G.M. Natural Products as Sources of New Drugs over the 30 Years from 1981 to 2010. J. Nat. Prod. 2012, 75, 311–335. [Google Scholar] [CrossRef] [PubMed]
- Ma, X.Q.; Shi, Q.; Duan, J.A.; Dong, T.T.X.; Tsim, K.W.K. Chemical analysis of Radix Astragali (Huangqi) in China: A comparison with its adulterants and seasonal variations. J. Agric. Food Chem. 2002, 50, 4861–4866. [Google Scholar] [CrossRef] [PubMed]
- Adesso, S.; Russo, R.; Quaroni, A.; Autore, G.; Marzocco, S. Astragalus membranaceus Extract Attenuates Inflammation and Oxidative Stress in Intestinal Epithelial Cells via NF-κB Activation and Nrf2 Response. Int. J. Mol. Sci. 2018, 19, 800. [Google Scholar] [CrossRef] [PubMed]
- Márquez-Flores, Y.K.; Villegas, I.; Cárdeno, A.; Rosillo, M.Á.; Alarcón-de-la-Lastra, C. Apigenin supplementation protects the development of dextran sulfate sodium-induced murine experimental colitis by inhibiting canonical and non-canonical inflammasome signaling pathways. J. Nutr. Biochem. 2016, 30, 143–152. [Google Scholar] [CrossRef] [PubMed]
- Amaral, A.; Ferreira, J.; Pinheiro, M.; Silva, J. Monograph of Himatanthus sucuuba, a Plant of Amazonian Folk Medicine. Pharmacogn. Rev. 2007, 1, 305–313. [Google Scholar]
- Rapa, S.; Di Paola, R.; Cordaro, M.; Siracusa, R.; D’Amico, R.; Fusco, R.; Autore, G.; Cuzzocrea, S.; Stuppner, H.; Marzocco, S. Plumericin Protects against Experimental Inflammatory Bowel Disease by Restoring Intestinal Barrier Function and Reducing Apoptosis. Biomedicines 2021, 9, 67. [Google Scholar] [CrossRef]
- Zhong, X.; Surh, Y.-J.; Do, S.-G.; Shin, E.; Shim, K.-S.; Lee, C.-K.; Na, H.-K. Baicalein Inhibits Dextran Sulfate Sodium-induced Mouse Colitis. J. Cancer Prev. 2019, 24, 129–138. [Google Scholar] [CrossRef] [PubMed]
- Pepe, G.; Rapa, S.; Salviati, E.; Bertamino, A.; Auriemma, G.; Cascioferro, S.; Autore, G.; Quaroni, A.; Campiglia, P.; Marzocco, S. Bioactive Polyphenols from Pomegranate Juice Reduce 5-Fluorouracil-Induced Intestinal Mucositis in Intestinal Epithelial Cells. Antioxidants 2020, 9, 699. [Google Scholar] [CrossRef]
- Alves, C.; Silva, J.; Pinteus, S.; Gaspar, H.; Alpoim, M.C.; Botana, L.M.; Pedrosa, R. From Marine Origin to Therapeutics: The Antitumor Potential of Marine Algae-Derived Compounds. Front. Pharmacol. 2018, 9, 777. [Google Scholar] [CrossRef]
- Ruocco, N.; Costantini, S.; Guariniello, S.; Costantini, M. Polysaccharides from the Marine Environment with Pharmacological, Cosmeceutical and Nutraceutical Potential. Molecules 2016, 21, 551. [Google Scholar] [CrossRef]
- Minhas, L.A.; Mumtaz, A.S.; Kaleem, M.; Waqar, R.; Annum, J. A Prospective Study on Morphological Identification and Characterization of Freshwater Green Algae Based on the Microscopic Technique in District Rawalpindi. Pak. J. Agric. Res. 2023, 36, 1–99. [Google Scholar] [CrossRef]
- Abdelrheem, D.A.; Abd El-Mageed, H.R.; Mohamed, H.S.; Rahman, A.A.; Elsayed, K.N.M.; Ahmed, S.A. Bis-indole alkaloid caulerpin from a new source Sargassum platycarpum: Isolation, characterization, in vitro anticancer activity, binding with nucleobases by DFT calculations and MD simulation. J. Biomol. Struct. Dyn. 2021, 39, 5137–5147. [Google Scholar] [CrossRef] [PubMed]
- Ma, M.; Fu, T.; Wang, Y.; Zhang, A.; Gao, P.; Shang, Q.; Yu, G. Polysaccharide from Edible Alga Enteromorpha clathrata Improves Ulcerative Colitis in Association with Increased Abundance of Parabacteroides spp. in the Gut Microbiota of Dextran Sulfate Sodium-Fed Mice. Mar. Drugs 2022, 20, 764. [Google Scholar] [CrossRef] [PubMed]
- Minhas, L.A.; Kaleem, M.; Farooqi, H.M.U.; Kausar, F.; Waqar, R.; Bhatti, T.; Aziz, S.; Jung, D.W.; Mumtaz, A.S. Algae-derived bioactive compounds as potential pharmaceuticals for cancer therapy: A comprehensive review. Algal Res. 2024, 78, 103396. [Google Scholar] [CrossRef]
- Chevolot, L.; Mulloy, B.; Ratiskol, J.; Foucault, A.; Colliec-Jouault, S. A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr. Res. 2001, 330, 529–535. [Google Scholar] [CrossRef]
- Spadaccini, M.; D’Alessio, S.; Peyrin-Biroulet, L.; Danese, S. PDE4 Inhibition and Inflammatory Bowel Disease: A Novel Therapeutic Avenue. Int. J. Mol. Sci. 2017, 18, 1276. [Google Scholar] [CrossRef] [PubMed]
- Mizoguchi, A.; Yano, A.; Himuro, H.; Ezaki, Y.; Sadanaga, T.; Mizoguchi, E. Clinical importance of IL-22 cascade in IBD. J. Gastroenterol. 2018, 53, 465–474. [Google Scholar] [CrossRef]
- Fukuyama, Y.; Kodama, M.; Miura, I.; Kinzyo, Z.; Kido, M.; Mori, H.; Nakayama, Y.; Takahashi, M. Structure of an anti-plasmin inhibitor, eckol, isolated from the brown alga Ecklonia kurome Okamura and inhibitory activities of its derivatives on plasma plasmin inhibitors. Chem. Pharm. Bull. 1989, 37, 349–353. [Google Scholar] [CrossRef] [PubMed]
- Gao, Z.; Han, Y.; Hu, Y.; Wu, X.; Wang, Y.; Zhang, X.; Fu, J.; Zou, X.; Zhang, J.; Chen, X.; et al. Targeting HO-1 by Epigallocatechin-3-Gallate Reduces Contrast-Induced Renal Injury via Anti-Oxidative Stress and Anti-Inflammation Pathways. PLoS ONE 2016, 11, e0149032. [Google Scholar] [CrossRef]
- Reddy, S.M.; Suresh, V.; Pitchiah, S.; Subramanian, B. Anti-inflammatory Activities of Sulfated Polysaccharides From Ethanol Crude Extract of Spyrida Species Red Seaweed. Cureus 2023, 15, e50284. [Google Scholar] [CrossRef] [PubMed]
- Lopes, D.; Melo, T.; Rey, F.; Meneses, J.; Monteiro, F.L.; Helguero, L.A.; Abreu, M.H.; Lillebø, A.I.; Calado, R.; Domingues, M.R. Valuing Bioactive Lipids from Green, Red and Brown Macroalgae from Aquaculture, to Foster Functionality and Biotechnological Applications. Molecules 2020, 25, 3883. [Google Scholar] [CrossRef]
- Kim, D.H.; Sung, B.; Kang, Y.J.; Jang, J.Y.; Hwang, S.Y.; Lee, Y.; Kim, M.; Im, E.; Yoon, J.-H.; Kim, C.M.; et al. Anti-inflammatory effects of betaine on AOM/DSS-induced colon tumorigenesis in ICR male mice. Int. J. Oncol. 2014, 45, 1250–1256. [Google Scholar] [CrossRef] [PubMed]
- Varani, J.; McClintock, S.D.; Nadeem, D.M.; Harber, I.; Zeidan, D.; Aslam, M.N. A multi-mineral intervention to counter pro-inflammatory activity and to improve the barrier in human colon organoids. Front. Cell Dev. Biol. 2023, 11, 1132905. [Google Scholar] [CrossRef]
- Liyanage, N.M.; Nagahawatta, D.P.; Jayawardena, T.U.; Jeon, Y.-J. The Role of Seaweed Polysaccharides in Gastrointestinal Health: Protective Effect against Inflammatory Bowel Disease. Life 2023, 13, 1026. [Google Scholar] [CrossRef]
- Feng, J.; Geng, J.; Wu, J.; Wang, H.; Liu, Y.; Du, B.; Yang, Y.; Xiao, H. A Potential Role of Plant/Macrofungi/Algae-Derived Non-Starch Polysaccharide in Colitis Curing: Review of Possible Mechanisms of Action. Molecules 2022, 27, 6467. [Google Scholar] [CrossRef]
- Besednova, N.N.; Zaporozhets, T.S.; Kuznetsova, T.A.; Makarenkova, I.D.; Kryzhanovsky, S.P.; Fedyanina, L.N.; Ermakova, S.P. Extracts and Marine Algae Polysaccharides in Therapy and Prevention of Inflammatory Diseases of the Intestine. Mar. Drugs 2020, 18, 289. [Google Scholar] [CrossRef] [PubMed]
- Repici, A.; Hasan, A.; Capra, A.P.; Scuderi, S.A.; Paterniti, I.; Campolo, M.; Ardizzone, A.; Esposito, E. Marine Algae and Deriving Biomolecules for the Management of Inflammatory Bowel Diseases: Potential Clinical Therapeutics to Decrease Gut Inflammatory and Oxidative Stress Markers? Mar. Drugs 2024, 22, 336. [Google Scholar] [CrossRef] [PubMed]
Algae | Phyla | In Vivo Models | Main Effects | Relevant Compounds | Concentration | Reference |
---|---|---|---|---|---|---|
Chlorella vulgaris | Chlorophyta | DSS-induced colitis | ↑ Regulatory T cells | Not investigated | 2 g/kg | [19] |
Caulerpa racemosa | Chlorophyta | DSS-induced colitis | ↓ TNF-α, IFN-γ, IL-6, IL-17, NFκB p65 ↑ IL-10 | Caulerpin | 40–4 mg/kg | [26] |
Ulva pertusa | Chlorophyta | DNBS-induced colitis | ↑ COX-2, iNOS, IL-4 ↓ NO, SOD, CAT, GSH, MDA, NF-κB signaling pathway | Not investigated | 10–50–100 mg/kg | [20] |
Ulva pertusa | Chlorophyta | DNBS-induced colitis | ↓ IL-6, IL-17, IL-23 ↑ IL-10 | Not investigated | 50–100 mg/kg | [21] |
Laminaria genus | Phaeophyta | Soybean-induced intestinal inflammation | ↓ Expression of inflammatory response-related genes | Alginate oligosaccharides, β-(1, 3)-glucan | 5% of the body weight | [25] |
Undaria pinnatifida | Phaeophyta | DNBS-induced colitis | ↓ H2O2, hydroxyl radicals ↑ •O−2 radical-scavenging activity | Fucoidan | 25% of the diet | [23] |
Not mentioned | Phaeophyta | Acetic acid-induced UC | ↓ PDE4, MDA, ONOO−, GSH ↑ AhR, Nrf2, HMOX1, GPx | Fucoidan | 150 mg/kg | [22] |
Macrocystis pyrifera | Phaeophyta | DSS-induced colitis | ↓ TNF-α, IL-1β, IL-6, IFN-γ, IL-1α, IL-3, IL-9, IL-12, MDA, MPO, NO, SOD, CAT | Fucoidan | 400 mg/kg | [24] |
Ecklonia cava | Phaeophyta | DSS-induced colitis | ↓ TNF-α, IL-1β, IL-6, NF-κB signaling pathway ↑ IL-10 | Eckol | 0.5–1.0 mg/kg | [27] |
Sargassum macrocarpum | Phaeophyta | DSS-induced colitis | ↓ MPO, TNF-α, IFN-γ, IL-1β, IL-17, MMP-2, MMP-9, MMP-13, NF-κB signaling pathway, iNOS | Sargahydroquinoic acid, sargachromeol, sargaquinoic acid | 12 mg/kg of the body weight | [29] |
Dictyopteris undulata | Phaeophyta | DSS-induced colitis | ↓ TNF-α, IL-6, iNOS, NO | Zonarol | 10–20 mg/kg | [30] |
Not mentioned | Phaeophyta | DSS-induced colitis | ↓ TNF-α, IL-1β, p65, COX-2, MDA, MPO ↑ Nrf2, HMOX1 | Dieckol | 5–10–15 mg/kg of body weight | [28] |
Turbinaria ornata | Phaeophyta | DSS-induced colitis | ↓ TNF-α, COX-2, MPO ↑ IL-10 | Steroids and sulfoquinovosyl monoacylglycerols | 15 mg/kg of body weight | [31] |
Porphyra tenera | Rhodophyta | DSS-induced colitis | ↓ TNF-α, IL-1β, IL-6, COX-2 ↑ Glycine betaine metabolism-related gut bacteria | Polyphenols | 500–1000 mg/kg of body weight | [32] |
Grateloupia turuturu | Rhodophyta | Not investigated | ↓ COX-2 | PUFAs | Five concentrations ranging between 12.5 and 250 μg mL−1 | [33] |
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Brizzi, A.; Rispoli, R.M.; Autore, G.; Marzocco, S. Anti-Inflammatory Effects of Algae-Derived Biomolecules in Gut Health: A Review. Int. J. Mol. Sci. 2025, 26, 885. https://doi.org/10.3390/ijms26030885
Brizzi A, Rispoli RM, Autore G, Marzocco S. Anti-Inflammatory Effects of Algae-Derived Biomolecules in Gut Health: A Review. International Journal of Molecular Sciences. 2025; 26(3):885. https://doi.org/10.3390/ijms26030885
Chicago/Turabian StyleBrizzi, Alessia, Rosaria Margherita Rispoli, Giuseppina Autore, and Stefania Marzocco. 2025. "Anti-Inflammatory Effects of Algae-Derived Biomolecules in Gut Health: A Review" International Journal of Molecular Sciences 26, no. 3: 885. https://doi.org/10.3390/ijms26030885
APA StyleBrizzi, A., Rispoli, R. M., Autore, G., & Marzocco, S. (2025). Anti-Inflammatory Effects of Algae-Derived Biomolecules in Gut Health: A Review. International Journal of Molecular Sciences, 26(3), 885. https://doi.org/10.3390/ijms26030885