Protective effect of marine animal hydrolysis-peptides on adjuvant-induced arthritis in mice by gut microbiota and short-chain fatty acids
), Xiurong Sua,b()Graphical Abstract
Abstract
Marine fauna provides a plentiful repository of peptides and bioactive proteins. Peptides and proteins isolated from marine animals have been studied and applied in the development of food supplements, drugs, and cosmeceutical products because of their special bioactivities, such as anti-inflammatory and antioxidant effects. This study focused on exploring the alleviating effects of five major marine animal-derived peptides (Apostichopus japonicus, Acaudina leucoprocta, Melanogrammus aeglefinus, Phascolosoma esculenta and Rhopilema esculentum) on adjuvant-induced arthritis (AIA). The treatment with five marine animals-derived peptides downregulated the expression levels of pro-inflammatory cytokines of interleukin (IL)-1β, IL-17 and tumor necrosis factor (TNF)-α in the bones of the mice with AIA and alleviated the rough surface of bone tissues significantly. A. japonicus-treatment ameliorates inflammation by restoring nuclear factor-κB pathway in AIA mice. High-throughput sequencing of the gut microbiota based on 16S rRNA sequencing revealed that A. japonicus peptide-treated AIA mice showed alterations and imbalance of intestinal flora and an increased abundance of Lactobacillus and Clostridium. Furthermore, metabolomic analysis showed that the level of short-chain fatty acids (SCFAs) in the feces was enhanced to different degrees in mice treated with five major marine animal-derived peptides. Taken together, we propose that major marine animal-derived peptides can alleviate arthritis by improving the imbalance in the gut flora and increasing SCFAs production to varying degrees.
Electronic Supplementary Material
References
J. Mitrović, S. Hrkač, J. Tečer, et al., Pathogenesis of extraarticular manifestations in rheumatoid arthritis: a comprehensive review, Biomedicines 11(5) (2023) 1262. https://doi.org/10.3390/biomedicines11051262.
A. Navrátilová, V. Bečvář, H. Hulejová, et al., New pro-inflammatory cytokine IL-40 is produced by activated neutrophils and plays a role in the early stages of seropositive rheumatoid arthritis, RMD Open. 9(2) (2023) e002894. https://doi.org/10.1136/rmdopen-2022-002894.
J. Zhao, S. Guo, S.J. Schrodi, et al., Molecular and cellular heterogeneity in rheumatoid arthritis: mechanisms and clinical implications, Front. Immunol. 12 (2021) 790122. https://doi.org/10.3389/fimmu.2021.790122.
G.R. Burmester, J.E. Pope, Novel treatment strategies in rheumatoid arthritis, Lancet 389 (2017) 2338-2348. https://doi.org/10.1016/S0140-6736(17)31491-5.
N.M. Hosny, D.M. Badary, M.S. Hareedy, A feasible HPTLC method for concurrent quantitation of allopurinol-montelukast co-therapy in plasma and evaluation of their hepatic and renal effects in rats: analytical, biochemical, and histopathological study, J. Pharm. Biomed. Anal. 233 (2023) 115439. https://doi.org/10.1016/j.jpba.2023.115439.
Mardani M, Mohammadshahi J, Abolghasemi S, et al., Drug-induced liver injury due to tofacitinib: a case report, J. Med. Case Rep. 17(1) (2023) 97. https://doi.org/10.1186/s13256-023-03821-4.
F. De Luca, Y. Shoenfeld, The microbiome in autoimmune diseases, Clin. Exp. Immunol. 195 (2019) 74-85. https://doi.org/10.1111/cei.13158.
T. Zhao, Y. Wei, Y. Zhu, et al., Gut microbiota and rheumatoid arthritis: from pathogenesis to novel therapeutic opportunities, Front. Immunol. 13 (2022) 1007165. https://doi.org/10.3389/fimmu.2022.1007165.
Y. Maeda, T. Kurakawa, E. Umemoto, et al., Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine, Arthritis Rheumatol. 68 (2016) 2646-2661. https://doi.org/10.1002/art.39783.
L. Jiang, M. Shang, S. Yu, et al., A high-fiber diet synergizes with Prevotella copri and exacerbates rheumatoid arthritis, Cell. Mol. Immunol. 19(12) (2022) 1414-1424. https://doi.org/10.1038/s41423-022-00934-6.
A. Pianta, S. Arvikar, K. Strle, et al., Evidence of the immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis, Arthritis Rheumatol. 69 (5) (2017) 964-975. https://doi.org/10.1002/art.40003.
H. Pan, R. Guo, Y. Ju, et al., A single bacterium restores the microbiome dysbiosis to protect bones from destruction in a rat model of rheumatoid arthritis, Microbiome 7(1) (2019) 107. https://doi.org/10.1186/s40168-019-0719-1.
E. Miyauchi, C. Shimokawa, A. Steimle, et al., The impact of the gut microbiome on extra-intestinal autoimmune diseases, Nat. Rev. Immunol. 23(1) (2023) 9-23. https://doi.org/10.1038/s41577-022-00727-y.
C. Hua, F. Buttgereit, B. Combe, Glucocorticoids in rheumatoid arthritis: current status and future studies, RMD Open. 6(1) (2020) e000536. https://doi.org/10.1136/rmdopen-2017-000536.
F. Ruiz-Ruiz, E. I. Mancera-Andrade, H.M.N. Iqbal, Marine-derived bioactive peptides for biomedical sectors: a review, Protein Pept. Lett. 24 (2017) 109-117. https://doi.org/10.2174/0929866523666160802155347.
F. Huang, Y. Jing, G. Ding, et al., Isolation and purification of novel peptides derived from sepia ink: effects on apoptosis of prostate cancer cell PC-3, Mol. Med. Rep. 16 (2017) 4222-4228. https://doi.org/10.3892/mmr.2017.7068.
F. Ruiz-Ruiz, E.I. Mancera-Andrade, H.M. Iqbal. Marine-derived bioactive peptides for biomedical sectors: a review, Protein Pept Lett. 24(2) (2017) 109-117. https://doi.org/10.2174/0929866523666160802155347.
H.K. Kang, H.H. Lee, C.H. Seo, et al., Antimicrobial and immunomodulatory properties and applications of marine-derived proteins and peptides, Mar. Drugs 17(6) (2019) 350. https://doi.org/10.3390/md17060350.
A. Sila, A. Bougatef, Antioxidant peptides from marine by-products: isolation, identification and application in food systems. a review, J. Funct. Foods 21 (2016) 10-26. https://doi.org/10.1016/j.jff.2015.11.007.
A. Hossain, D. Dave, F. Shahidi. Antioxidant potential of sea cucumbers and their beneficial effects on human health, Mar. Drugs 20(8) (2022) 521. https://doi.org/10.3390/md20080521.
Z. Lu, N. Sun, L. Dong, et al., Production of bioactive peptides from sea cucumber and its potential health benefits: a comprehensive review, J. Agric. Food Chem. 70(25) (2022) 7607-7625. https://doi.org/10.1021/acs.jafc.2c02696.
Y. Wang, X. Gao, J. Zhou, et al., Studies on the hypolipidemic function of Acaudina leucoprocta hydrolyzate hydrolysed by Bacillus licheniformis, J. Chin. Inst. Food Sci. Technol. 17 (2017) 44-50. https://doi.org/10.16429/j.1009-7848.2017.04.006.
Q. Zhu, H. Zhuo, L. Yang, et al., A peptide HEPFYGNEGALR from Apostichopus japonicus alleviates acute alcoholic liver injury by enhancing antioxidant response in male C57BL/6J mice, Molecules 27(18) (2022) 5839. https://doi.org/10.3390/molecules27185839.
L. Qi, X. Zhang, X. Wang, Heparin inhibits the inflammation and proliferation of human rheumatoid arthritis fibroblast-like synoviocytes through the NF-κB pathway, Mol. Med. Rep. 14 (2020) 3743-3748. https://doi.org/10.3892/mmr.2016.5719.
S. Sudirman, C.Y. Chen, C.K. Chen, et al., Fermented jellyfish (Rhopilema esculentum) collagen enhances antioxidant acvtivity and cartilage protection on surgically induced osteoarthritis in obese rats, Front. Pharmacol, 14 (2023) 1117893. https://doi.org/10.3389/fphar.2023.1117893.
J. Li, Q. Li, J. Li, et al., Peptides derived from Rhopilema esculentum hydrolysate exhibit angiotensin converting enzyme (ACE) inhibitory and antioxidant abilities, Molecules 19(9) (2014) 13587-13602. https://doi.org/10.3390/molecules190913587.
X. Liu, M. Zhang, C. Zhang, et al., Angiotensin converting enzyme (ACE) inhibitory, antihypertensive and antihyperlipidaemic activities of protein hydrolysates from Rhopilema esculentum, Food Chem. 134 (2012) 2134-2140. https://doi.org/10.1016/j.foodchem.2012.04.023.
L. Xiao, S. Liu, Q. He, et al., The acute toxicity and hematological characterization of the effects of tentacle-only extract from the jellyfish Cyanea capillata, Mar. Drugs 9 (2011) 526-534. https://doi.org/10.3390/md9040526.
H. Wong, L. Liu, W. Ouyang, et al., Exposure-effect relationships in established rat adjuvant-induced and collagen-induced arthritis: a translational pharmacokinetic-pharmacodynamic analysis, J. Pharmacol. Exp. Ther. 369(3) (2019) 406-418. https://doi.org/10.1124/jpet.118.255562.
J. Han, S.S. Tang, Y.Y. Li, et al., In silico analysis and in vivo tests of the tuna dark muscle hydrolysate anti-oxidation effect, RSC Adv. 8 (2018) 14109-14119. https://doi.org/10.1039/c8ra00889b.
Z. Zhang, H.T. Wan, J.J. Han, et al., Ameliorative effect of tuna elastin peptides on AIA mice by regulating the composition of intestinal microorganisms and SCFAs, J. Funct. Foods 92 (2022) 105076. https://doi.org/10.1016/j.jff.2022.105076.
K.J. Livak, T.D. Schmittgen, Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method, Methods 25(4) (2001) 402-408. https://doi.org/10.1006/meth.2001.1262.
L. Tan, J.U. Huangxian, L.I. Jieshou, Extraction and determination of short-chain fatty acids in biological samples, Chinese Journal of Chromatography 24(1) (2006) 81-87. https://doi.org/10.1016/S1872-2059(06)60004-7.
G. Frazzei, A. Musters, N. de Vries, et al., Prevention of rheumatoid arthritis: a systematic literature review of preventive strategies in at-risk individuals, Autoimmun. Rev. 22(1) (2023) 103217. https://doi.org/10.1016/j.autrev.2022.103217.
X. Cai, X.M. Chen, X. Xia, et al., The bone-protecting efficiency of chinese medicines compared with western medicines in rheumatoid arthritis: a systematic review and meta-analysis of comparative studies, Front. Pharmacol. 9 (2018) 914. https://doi.org/10.3389/fphar.2018.00914.
X. Zhao, S. Jiang, Q. Dong, et al., Anti-rheumatoid arthritis effects of iridoid glucosides from Lamiophlomis rotata (Benth.) kudo on adjuvant-induced arthritis in rats by OPG/RANKL/NF-κB signaling pathways, J. Ethnopharmacol. 266 (2021) 113402. https://doi.org/10.1016/j.jep.2020.113402.
C.E.C.C. Ejike, T.P.C. Ezeorba, O. Ajah, et al., Big things, small packages: an update on microalgae as sustainable sources of nutraceutical peptides for promoting cardiovascular health, Glob. Chall. 7(5) (2023) 2200162. https://doi.org/10.1002/gch2.202200162.
S. Nalinanon, S. Benjakul, H. Kishimura, et al., Functionalities and antioxidant properties of protein hydrolysates from the muscle of ornate threadfin bream treated with pepsin from skipjack tuna, Food Chem. 124(4) (2011) 1354-1362. https://doi.org/10.1016/j.foodchem.2010.07.089.
Y. Wu, H. Jiang, J.S. Lin, et al., Antioxidant, hypolipidemic and hepatic protective activities of polysaccharides from Phascolosoma esculenta, Mar. Drugs. 18(3) (2020) 158. https://doi.org/10.3390/md18030158.
S. Zhao, Q. Cheng, Q. Peng, et al., Antioxidant peptides derived from the hydrolyzate of purple sea urchin (Strongylocentrotus nudus) gonad alleviate oxidative stress in Caenorhabditis elegans, J. Funct. Foods 48 (2018) 594-604. https://doi.org/10.1016/j.jff.2018.07.060.
A. Guru, C. Lite, A.J. Freddy, et al., Intracellular ROS scavenging and antioxidant regulation of WL15 from cysteine and glycine-rich protein 2 demonstrated in zebrafish in vivo model, Dev. Comp. Immunol. 114 (2021) 103863. https://doi.org/10.1016/j.dci.2020.103863.
S. Umayaparvathi, S. Meenakshi, V. Vimalraj, et al., Antioxidant activity and anticancer effect of bioactive peptide from enzymatic hydrolysate of oyster (Saccostrea cucullata), Biomed. Prev. Nutr. 4 (2014) 343-353. https://doi.org/10.1016/j.bionut.2014.04.006.
G. Feng, L.S. Lai, S. Chen, et al., In vitro and in vivo immunoregulatory activity of sulfated fucan from the sea cucumber A. leucoprocta, Int. J. Biol. Macromol. 187 (2021) 931-938. https://doi.org/10.1016/j.ijbiomac.2021.08.008.
S. Fan, Y. Huang, G. Lu, et al., Novel anti-hyperuricemic hexapeptides derived from Apostichopus japonicus hydrolysate and their modulation effects on the gut microbiota and host microRNA profile, Food Funct. 13(7) (2022) 3865-3878. https://doi.org/10.1039/d1fo03981d.
J.E. Kim, H.J. Hur, K.W. Lee, et al., Anti-inflammatory effects of recombinant arginine deiminase originating from Lactococcus lactis ssp. lactis ATCC 7962, J. Microbiol. Biotechnol. 17(9) (2007) 1491-1497.
G.B. Berikol, G. Berikol, C. Ayrik, et al., Antioxidant and neuroprotective effects of L-arginine administration after traumatic brain injury and hemorrhagic shock in rats, Turk Neurosurg. 33(3) (2023) 379-385. https://doi.org/10.5137/1019-5149.JTN.35263-21.2.
W. Feng, H. Ao, C. Peng, et al., Gut microbiota, a new frontier to understand traditional Chinese medicines, Pharmacol. Res. 142 (2019) 176-191. https://doi.org/10.1016/j.phrs.2019.02.024.
Z. Du, J. Wang, Y. Lu, et al., The cardiac protection of Baoyuan decoction via gut-heart axis metabolic pathway, Phytomedicine 79 (2020) 153322. https://doi.org/10.1016/j.phymed.2020.153322.
M.X. Chen, S.Y. Wang, C.H. Kuo, et al., Metabolome analysis for investigating host-gut microbiota interactions, J. Formos. Med. Assoc. 118 (2019) S10-S22. https://doi.org/10.1016/j.jfma.2018.09.007.
G. Horta-Baas, A. Sandoval-Cabrera, M.D.S. Romero-Figueroa, Modification of gut microbiota in inflammatory arthritis: highlights and future challenges, Curr Rheumatol. Rep. 23(8) (2021) 67. https://doi.org/10.1007/s11926-021-01031-9.
J.Y. Noh, C.S. Wu, J.A.A. DeLuca, et al., Novel role of Ghrelin receptor in gut dysbiosis and experimental colitis in aging, Int. J. Mol. Sci. 23(4) (2022) 2219. https://doi.org/10.3390/ijms23042219.
J.Y. Lee, M. Mannaa, Y. Kim, et al., Comparative analysis of fecal microbiota composition between rheumatoid arthritis and osteoarthritis patients, Genes 10(10) (2019) 748. https://doi.org/10.3390/genes10100748.
N.A. Alsharairi, Therapeutic potential of gut microbiota and its metabolite short-chain fatty acids in neonatal necrotizing enterocolitis, Life 13(2) (2023) 561. https://doi.org/10.3390/life13020561.
M. Zhang, Y. Wang, X. Zhao, et al., Mechanistic basis and preliminary practice of butyric acid and butyrate sodium to mitigate gut inflammatory diseases: a comprehensive review, Nutr. Res. 95 (2021) 1-18. https://doi.org/10.1016/j.nutres.2021.08.007.
P. Li, G. Chen, J. Zhang, et al., Live Lactobacillus acidophilus alleviates ulcerative colitis via the SCFAs/mitophagy/NLRP3 inflammasome axis, Food Funct. 13(5) (2022) 2985-2997. https://doi.org/10.1039/d1fo03360c.
Y. Zhou, F. Zhang, L. Mao, et al., Bifico relieves irritable bowel syndrome by regulating gut microbiota dysbiosis and inflammatory cytokines, Eur. J. Nutr. 62 (2023) 139-155. https://doi.org/10.1007/s00394-022-02958-0.
M.C. Choi, J. Jo, J. Park, et al., NF-κB signaling pathways in osteoarthritic cartilage destruction, Cells 8(7) (2019) 734. https://doi.org/10.3390/cells8070734.
Q. Guo, M. Zhang, Y. Dong, et al., Isobavachalcone ameliorates the progression of osteoarthritis by suppressing NF-κB signaling pathway, Int. Immunopharmacol. 119 (2023) 110102. https://doi.org/10.1016/j.intimp.2023.110102.
A.I.S. Jrad, M. Trad, W. Bzeih, et al., Role of pro-inflammatory interleukins in osteoarthritis: a narrative review, Connect Tissue Res. 64(3) (2023) 238-247. https://doi.org/10.1080/03008207.2022.2157270.
京公网安备11010802044758号