Marine Algae and Deriving Biomolecules for the Management of Inflammatory Bowel Diseases: Potential Clinical Therapeutics to Decrease Gut Inflammatory and Oxidative Stress Markers?
Abstract
:1. Introduction
2. Search Strategy
Methods
3. Pathophysiology of IBD
4. Inflammatory and Oxidative Stress Markers Related to IBD
4.1. Cytokines Related to the Inflammatory Response in IBD
4.2. NF-κB Pathway in IBD
4.3. Oxidative Stress Markers in IBD
4.4. Trefoil Factor 3 (TFF3)
4.5. Lactoferrin
4.6. SIRT1
5. Marine Ecosystem: A Useful Tool in the Management of IBD Symptomatology
5.1. Focusing on Marine Algae in the Treatment of IBD
5.1.1. Macroalgae
5.1.2. Microalgae
6. Pharmacokinetic Properties of Marine Algae-Derived Compounds
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Type of Algae | Study Design and Concentrations | In Vitro Cell Type | Control | Main Finding | Mechanisms | Reference |
---|---|---|---|---|---|---|
Korean seaweeds, Ulva pertusa polysaccharide (UPP) | 1.5 × 106 cells/well of LS174T and Caco-2 was incubated for 24 h (5 % CO2, 37 °C). UUP (1, 10, and 100 μg/mL) were added to the cells and incubated for 24 h. Total mRNA was obtained for further analysis. Culture media was used as a negative control (NC), and propionic acid (5 mM) as a positive control (PC). | LS174T and Caco-2 cells | Culture media, propionic acid 5 mM | ↑ mRNA expression of MUC2, ZO-1, occludin, and TFF3 | Strength Tight junction (TJ) and proliferation and survival of the epithelial cells. | [94] |
Fucoidan, a sulfated polysaccharide from brown algae | Caco-2 cells were seeded at 3.75 × 105 cells/well, the culture media was changed every 3 days until the cells fully differentiated, and the cells were used in passage number 48–62. RAW264.7 cells were seeded at 8.5 × 106 cells/well and were used in passage number 10–30, 1.5 fucoidan (500 µg/mL) was applied to the apical side for 3 h and LPS 100 ng·mL was added to the basolateral side and after additional 3 h, the basolateral supernatant was collected to be used for marker analysis. | co-cultured Caco-2 and RAW264.7 | Budesonide 1 µM and TNF- α 50 µg/mL | ↓ mRNA expression of IL-8, TNF-α | Inhibition of TNF-α secretion resulted from LPS-stimulated RAW246.7. | [113] |
Zonarol extracted from the brown algae, Dictyopteris undulata | RAW246.7 cells were seeded at 1 × 105 cell/cm2, and after 24 h LPS 10µg/mL was added with or without zonarol 2 µM, 24 h later the cells were subjected to the required assay. | RAW264.7 | The cells not treated by LPS or zonarol were used as a normal control | ↓ NO, IL-1b, IL-6 and iNOS | Inhibit the inflammatory reaction in the macrophage cell line | [98] |
Type of Algae | Study Design and Dose | Model | Inducer/Control | Main Findings | Mechanisms | Reference |
---|---|---|---|---|---|---|
Korean seaweeds, Ulva pertusa polysaccharide (UPP) | Oral prophylactic Administration of UPP at doses (50, 100, and 200 mg/kg) once daily for three weeks After UPP administration, a 5% dextran sulfate sodium (DSS) was administered for the next eight days to induce UC | Mouse model | Dextran sulfate sodium, mesalazine (100 mg/kg) | ↑ IL-4, IL-10, and IgA, occludin, and claudin-1 ↓ IL-1β, TNF-α, iNOS, IL-6, MPO, ERK, and p38 phosphorylation | Interfere with MAPK and NF-κB signaling pathway leading to inhibition of the inflammatory response-associated signaling pathways. | [94] |
Depyrogenated fucoidan (DPF) and fucoidan-polyphenol complex (Maritech Synergy) extracted from Fucus vesiculosus | UC was induced by using DSS in the drinking water from day 1 to day 8. then the treatment group received two fucoidan extracts for 7 days, either by oral Synergy or DPF) or intraperitoneal (DPF). | Male C57BL/6 mice | Dextran sulfate sodium/no positive control, the mice that didn’t receive SSD were a healthy control | IP DPF, ↓ −36.4% IL-1α, −28.6% IL-1β, −31.1% IL-10, −52.8% MIP-1α, −43.7% G-GSF, MCP-1 (%NA) and ↑ 58.6% IFN- γ, 115.8% RANTES. Oral DPF, ↓ −55.9% IL-1α, −51.2% IL-1β, −62.2% IL-10, −46.5% MIP-1α, −60.0% MIP-1β, −80.6% G-CSF and −51.0% GM-GSF. Oral Synergy, ↓ −71.3% IL-1α, −55.7% IL-1β, −50.7% IL-3, −69.2% IL-10, −26.5% IL-12(P40), −29.4% IL-12 (P70), −30.8% IL-13, −60.9% MIP-1α, −72.7% MIP-1β, −85.2% G-CSF and −51.9% GM-GSF, −36.6% Exotaxin, and −68.0% TNF- α. | Affect pro-inflammatory signaling and macrophage pathways such as p38, Erk, JNK, HMGB1, and NF-κB. | [56] |
Hydroquinone zonarol from Dictyopteris undulata (brown algae) | 2% of DSS was used in drinking water for 14 days and at the same time 5-aminosalicylic acid (5-ASA at a dose of 50 mg/kg, and/or zonarol at doses of 10 and 20 mg/kg were used orally once a day for 14 days. | Male Slc:ICR mice | Dextran sulfate sodium/5-ASA 50 mg/kg as a positive control | ↓ 44.4% TNF-α, 15.2% IL-1β, 21.5% iNOS, 28.1%, TUNEL+ | Inhibit the TNF-α signaling pathway. | [98] |
polysaccharide-rich extract from Eucheuma cottonii (EC) | 2.5% (w/v) DSS was used in drinking water for 7 days, at the same time, EC at the dose 0.35; 0.70; or 1.75 g/kg, and curcumin 0.10 g/kg was orally delivered once per day of DSS treatment for 7 days. | male BALB/c mice | dextran sulfate sodium/curcumin 0.10 g/kg as a positive control | ↓ TNF-α, IL-1β, and IL-6 in serum | Block TNF-α signaling pathway. | [100] |
sulfated polysaccharide (PLS) from Hypnea musciformis | The animals were pretreated orally with PLS (10, 30, and 60 mg/kg, for three days, or dexamethasone (1 mg/kg, s.c.) then trinitrobenzene sulfonic acid (TNBS) was administered as a single intracolonic | male Wistar rats | trinitrobenzene sulfonic acid (TNBS) in a 50% ethanol/Dexamethasone (1 mg/kg, s.c.) as a positive control | ↑ 246.3% GSH ↓ 46.8% MDA, 220% NO2/NO3, 22.7% IL-1β, and 27.4% TNF-α | Inhibit the synthesis and release of the product of the Inflammation. | [101] |
β-glucans derivedfrom seaweeds Laminaria hyperborea and Laminariadigitata | The animals were divided into 4 dietary groups (i) basal diet (BD), (ii) BD + β-glucans from Laminaria hyperborea, (iii) BD + β-glucans from Laminaria digitata, and (iv) BD + β-glucans from Saccharomyces cerevisiae. | Pigs | NA | ↓ IL-17a, IL-17F, IL-22, IL-23R, IL-5, IL-6 in S. cerevisiae group. ↓ IL-17a, IL-22, IL-23R, IL-10, IL-6 in L. digitata group. ↓ IL-17a, IL-17F, IL-22, IL-23R, IL-6 in L. hyperborea group. | Modulate the Th17 pathways without affecting TREG pathways. | [102] |
Ulva pertusa (green alga) | 2,4,6-dinitrobenzene sulphonic acid (DNBS in 50% ethanol was administered intrarectal as a single dose to induce colitis. Then Ulva Pertusa extract was administered orally for 4 days. | male CD1 mice | 2,4,6-dinitrobenzene sulphonic acid (DNBS)/the control group treated with saline | ↓ nitrotyrosine, Bax/Bcl-2 ratio, mast cell infiltration, NF-κB, IL-5, IL-9, IL13, iNOS, COX2, P53, Bax, Caspase-3, Caspase-8, Caspase-9, MDA, ↑ IκBα, IL-4, Bcl-2, Nrf2, GSH, CAT, SOD, SIRT1, Mn-SOD, HO-1 | Modulate Nrf2/SIRT1 and NF-κB pathway. | [103] |
polysaccharide extracted from Enteromorpha clathrate (EPC) | dextran sulfate sodium (DSS) in 2.0% (w/v) in drinking water for 8 days, at the same time EPC at a dosage of 100 mg/kg/day was used orally. | male c57bl/6j mice | dextran sulfate sodium (DSS)/normal control group which serves as the baseline for comparison. | No markers evaluated in this study | N.A | [107] |
Ulva pertusa (green alga) | 2,4,6-dinitrobenzene sulphonic acid (DNBS in 50% ethanol was administered intrarectal as a single dose to induce colitis. Then Ulva Pertusa extract was administered orally for 4 days. | Male CD1 mice | 2,4,6-dinitrobenzene sulphonic acid (DNBS)/the control group treated with saline | ↓ ICAM)-1 and p-Selectin, CD68, CD4, CD8, TLR4, MYD88, TRAF6, NLRP3, ASC, Caspase-1 ↓ IL-6, IL-17, and IL-23 in the serum ↑ serum IL-10 | Modulate TLR4/Myd88/TRAF6 Pathway and NLPR3 inflammasome. | [106] |
Low Molecular Weight Sulfate Ulva Polysaccharide (LMW-ulvan) from Ulva pertusa | 2% (w/v) DSS drinking water for 5 days, then LMW-ulvan at doses 50 and 100 mg/kg was administered orally for 7 days | Male C57BL/6 SPF mice | dextran sulfate sodium (DSS)/5-ASA (50 mg/kg) | ↑ IL-4, CAT, GPx enzyme activity, occludin, ZO-1, Claudin-1↓ IL-1β, IFN-γ, and MDA in serum and colon | Suppress NLRP3 inflammasome activation, inhibit Th1 cell response, and enhance antioxidant defense system. | [104] |
Laminaria japonica extract (LJE) | 5% DSS in drinking water for 7 days, during the same time LJE was administered orally twice a day at doses of 100 and 300 mg/kg with probiotics at a dose of 300 mg/kg. | Male Balb/c mice | dextran sulfate sodium/normal animals were used as a control group | ↓ IL-1β, IL-6, TNF-α, IL-17, IL-12 (P40) | Modulate Th17 and Th1/Th17 dependent pathway | [108] |
Chlorella vulgaris (C.V) (green algae) | 2.5% (w/v) DSS in drinking water for 7 days. Then C. vulgaris extract was orally administered 2 g/kg for 3 weeks | female C57BL/6 mice | dextran sulfate sodium/normal animals without treatment used as a control group | ↑ Treg, short-chain fatty acid (SCFAs), absolute CD4 + Foxp3+, Rort + Foxp3+ regulatory cells, and CD4+ T cells in the spleen and mouse lymph node | Improve immune tolerance by immune regulatory mechanisms mediated by Tregs and modulate the microbiome. | [111] |
Caulerpa mexicana extract (green algae) | 3% DSS in drinking water for 14 days. During this period, the Caulerpa mexicana methanolic extract (2 mg/kg/day) was administered intravenously on alternate days | Male BALB/c mice | dextran sodium sulfate/control group received only saline without the DSS or the algae extract, serving as a baseline for comparison | ↓ Th1, Th17, IL-6, IL-12, TNF-α, IFN-γ, and IL-17 | Modulate Th1 and Th17 pathway. | [109] |
Spirulina platensis (SP), Dunaliella salina (DS) | After sedating the animals by IP injection of pentobarbitone (35 mg/kg), acetic acid (4%, v/v) in saline was infused for 30 s into the colon to a distance of 8c cm using a polyethylene tube (2 mm) at the day 16, SP and DS was administered orally for 15 consecutive days with dose 500 mg/kg, in another group sulfasalazine was administered orally with dose 500 mg/kg at 13th, 14th, and 15th days. | Male Wistar albino rats | 4% v/v acetic acid (AA)/normal control group received only saline, the group with a single dose of AA without treatment served as a positive control group, another group received sulfasalazine | ↑ GSH, CAT, SOD ↓ MDA, PCO, MPO, TNF-α, IL-1β, IL-6, PEG2 | Scavenge free radicals and decrease Infiltration of Inflammatory cells. | [112] |
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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. https://doi.org/10.3390/md22080336
Repici A, Hasan A, Capra AP, Scuderi SA, 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? Marine Drugs. 2024; 22(8):336. https://doi.org/10.3390/md22080336
Chicago/Turabian StyleRepici, Alberto, Ahmed Hasan, Anna Paola Capra, Sarah Adriana Scuderi, Irene Paterniti, Michela Campolo, Alessio Ardizzone, and Emanuela Esposito. 2024. "Marine Algae and Deriving Biomolecules for the Management of Inflammatory Bowel Diseases: Potential Clinical Therapeutics to Decrease Gut Inflammatory and Oxidative Stress Markers?" Marine Drugs 22, no. 8: 336. https://doi.org/10.3390/md22080336