Hostname: page-component-76d6cb85b7-2r2wp Total loading time: 0 Render date: 2026-07-14T21:32:46.565Z Has data issue: false hasContentIssue false
  • English
  • Français

The prophylactic and therapeutic impact of Trichinella spiralis larvae excretory secretory antigens- loaded Ca-BTC metal organic frameworks on induced murine colitis

Published online by Cambridge University Press:  24 May 2024

E.M. Fawzy ,
M.A. Selim ,
N. E. Mostafa ,
R.M. Abdelhameed ,
A.M. Darwish ,
A.M. Yousef ,
M.A. Alabiad ,
M.N. Ibrahim ,
H.M. Fawzy  and
E.F. Abdel Hamed Open the ORCID record for E.F. Abdel Hamed [Opens in a new window]
E.M. Fawzy
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
M.A. Selim
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
N. E. Mostafa
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
R.M. Abdelhameed
Affiliation:
Department of Applied Organic Chemistry, National Research Centre, Dokki, Giza, Egypt
A.M. Darwish
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
A.M. Yousef
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
M.A. Alabiad
Affiliation:
Department of Pathology, Faculty of Medicine, Zagazig University, Egypt
M.N. Ibrahim
Affiliation:
Department of Clinical Laboratories, College of applied Medical Sciences, Jouf University, Qurrayat 77451, KSA
H.M. Fawzy
Affiliation:
Department of Community, Faculty of Medicine, Zagazig University, Sharkia, Egypt
E.F. Abdel Hamed*
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Sharkia, Egypt
*
Corresponding author: E.F. Abdel Hamed; Email: drenasfakhry@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Background: Inflammatory bowel disease is an autoimmune disease that affects the gut. T. spiralis larvae (E/S Ags) loaded on calcium-benzene-1,3,5-tricarboxylate metal-organic frameworks (Ca-BTC MOFs) were tested to determine whether they might prevent or cure acetic acid-induced murine colitis. Methods: T. spiralis larvae E/S Ags/Ca-BTC MOFs were used in prophylactic and therapeutic groups to either precede or follow the development of murine colitis. On the seventh day after colitis, mice were slaughtered. The effect of our target antigens on the progress of the colitis was evaluated using a variety of measures, including survival rate, disease activity index, colon weight/bodyweight, colon weight/length) ratios, and ratings for macroscopic and microscopic colon damage. The levels of inflammatory cytokines (interferon-γ and interleukin-4), oxidative stress marker malondialdehyde, and glutathione peroxidase in serum samples were evaluated. Foxp3 T-reg expression was carried out in colonic and splenic tissues. Results: T. spiralis larvae E/S Ags/Ca-BTC MOFs were the most effective in alleviating severe inflammation in murine colitis. The survival rate, disease activity index score, colon weight/length and colon weight/bodyweight ratios, and gross and microscopic colon damage scores have all considerably improved. A large decrease in proinflammatory cytokine (interferon-γ) and oxidative stress marker (malondialdehyde) expression and a significant increase in interleukin-4 and glutathione peroxidase expression were obtained. The expression of Foxp3+ Treg cells was elevated in colonic and splenic tissues. Conclusion: T. spiralis larvae E/S Ags/Ca-BTC MOFs had the highest anti-inflammatory, antioxidant, and cytoprotective capabilities against murine colitis and might be used to develop new preventative and treatment strategies.

Keywords

IBDT. spiralisExcretory-secretory antigensMOFsGSH-Px

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e41
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Alzoghaibi, MA (2013) Concepts of oxidative stress and antioxidant defense in Crohn’s disease. World Journal of Gastroenterology 19(39), 6540. https://doi.org/10.3748/wjg.v19.i39.6540CrossRefGoogle ScholarPubMed
Ansari, MN, Rehman, NU, Karim, A, Soliman, GA, Ganaie, MA, Raish, M, and Hamad, AM (2021) Role of oxidative stress and inflammatory cytokines (TNF-α and IL-6) in acetic acid-induced ulcerative colitis in rats: ameliorated by otostegiafruticosa. Life (Basel, Switzerland) 11(3), 195. https://doi.org/10.3390/life11030195Google Scholar
Ashour, DS, Othman, AA, Shareef, MM, Gaballah, HH, and Mayah, WW (2014) Interactions between Trichinella spiralis infection and induced colitis in mice. Journal of Helminthology 88(2), 210. https://doi.org/10.1017/s0022149x13000059CrossRefGoogle ScholarPubMed
Beard, JA, Franco, DL, and Click, BH (2020) The Burden of Cost in Inflammatory Bowel Disease: A Medical Economic Perspective and the Future of Value-Based Care. Curr Gastroenterol Rep 22(2), 6 doi: 10.1007/s11894-020-0744-z.CrossRefGoogle Scholar
Boehm, D, Krzystek-Korpacka, M, Neubauer, K, Matusiewicz, M, Paradowski, L, and Gamian, A (2012) Lipid peroxidation markers in Crohn’s disease: the associations and diagnostic value. Clinical Chemistry and Laboratory Medicine 50(8), 1359–1366. https://doi.org/10.1515/cclm-2011-0817CrossRefGoogle ScholarPubMed
Bou-Fersen, AM, Anim, JT, and Khan, I (2008) Experimental colitis is associated with ultrastructural changes in inflamed and uninflamed regions of the gastrointestinal tract. Medical Principles and Practice 17(3), 190–196 https://doi.org/10.1159/000117791CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1-2), 248–254. https://doi.org/10.1006/abio.1976.9999CrossRefGoogle ScholarPubMed
Buitrago, G, Pickering, D, Ruscher, R, Caceres, CC, Jones, L, Cooper, M, and Loukas, A ( 2021) A netrin domain-containing protein secreted by the human hookworm Necator americanus protects against CD4 T cell transfer colitis. Translational Research 232, 88–102. https://doi.org/10.1016/j.trsl.2021.02.012CrossRefGoogle ScholarPubMed
Chamanara, M, Abdollahi, A, Rezayat, SM, Ghazi-Khansari, M, Dehpour, A, Nassireslami, E, and Rashidian, A (2019) Thymol reduces acetic acid-induced inflammatory response through inhibition of NF-kB signaling pathway in rat colon tissue. Inflammopharmacology 27(6), 1275–1283. https://doi.org/10.1007/s10787-019-00583-8CrossRefGoogle ScholarPubMed
Chaney, AL and Marbach, EP (1962) Modified reagents for determination of urea and ammonia. Clinical Chemistry, 8(2): 130–132. https://doi.org/10.1093/clinchem/8.2.130CrossRefGoogle ScholarPubMed
Cleenewerk, L, Garssen, J, and Hogenkamp, A (2020) Clinical use of Schistosoma mansoni antigens as novel immunotherapies for autoimmune disorders. Frontiers in Immunology 11, 1821. https://doi.org/10.3389/fimmu.2020.01821CrossRefGoogle ScholarPubMed
Corfixen, NL (2017) PRObiotic Treatment of Ulcerative Colitis patients with Trichuris suis Ova (PROCTO). International Journal for Parasitology: Parasites and Wildlife 6(3): 139–145. https://plen.ku.dk/english/research/organismal_biology/hp/research-themesprojects/probiotic-treatment-of-ulcerative-colitis-patients-with-trichuris-suis-ova-procto/Google Scholar
Cvetkovic, J, Ilic, N, Gruden-Movsesijan, A, Tomic, S, Mitic, N, Pinelli, E, and Sofronic-Milosavljevic, L (2020) Signalling induced by Trichinella spiralis products contributes to the tolerogenic signatures of human dendritic cells. Science Reports 10, 20283. https://doi.org/10.1038/s41598-020-77497-x.CrossRefGoogle Scholar
Derda, M, Wandurska-Nowak, E, and Hadaś, E (2004) Changes in the level of antioxidants in the blood from mice infected with Trichinella spiralis. Parasitology Research, 93: 207–210. doi: 10.1007/s00436-004-1093-9.CrossRefGoogle ScholarPubMed
El-Shahat, M and Abdelhameed, RM (2022) Metal precursors from eggshells wastes for the production of calcium–organic frameworks and their use in accelerating the formation of carbon–carbon bonds. Applied Catalysis A: General, 635, 118558. https://doi.org/10.1016/j.apcata.2022.118558.CrossRefGoogle Scholar
Fabia, R, Willen, R, Ar’Rajab, A, Andersson, R, Ahren, B, and Bengmark, S (1992) Acetic acid-induced colitis in the rat: a reproducible experimental model for acute ulcerative colitis. European Surgical Research 24(4), 211–225. https://doi.org/10.1159/000129209CrossRefGoogle Scholar
Gratton, SE, Ropp, PA, Pohlhaus, PD, Luft, JC, Madden, VJ, Napier, ME, and DeSimone, JM (2008) The effect of particle design on cellular internalization pathways. Proceedings of the National Academy of Sciences 105(33), 11613–11618. doi: 10.1073/pnas.0801763105.CrossRefGoogle ScholarPubMed
Hamouda, HE, Zakaria, SS, Ismail, SA, Khedr, MA, and Mayah, WW (2011) p53 antibodies, metallothioneins, and oxidative stress markers in chronic ulcerative colitis with dysplasia. World Journal of Gastroenterology 17(19), 2417. https://doi.org/10.3748/wjg.v17.i19.2417CrossRefGoogle ScholarPubMed
Hidalgo, T, Simón-Vázquez, R, González-Fernández, A, and Horcajada, P (2022) Cracking the immune fingerprint of metal–organic frameworks. Chemical Science 13(4), 934–944. https://doi.org/10.1039/D1SC04112FCrossRefGoogle ScholarPubMed
Ilic, N, Kosanović, M, Gruden-Movsesijan, A, Glamočlija, S, Sofronić-Milosavljević, L, Čolić, M, and Tomić, S (2021) Harnessing immunomodulatory mechanisms of Trichinella spiralis to design novel nanomedical approaches for restoring self-tolerance in autoimmunity. Immunology Letters 238, 57–67. https://doi.org/10.1016/j.imlet.2021.04.012CrossRefGoogle ScholarPubMed
Jeengar, MK, Thummuri, D, Magnusso, M, Naidu, VGM, and Uppugunduri, S (2017) Uridine ameliorates dextran sulfate sodium (DSS)-induced colitis in mice. Science Reports 7(1), 3924. https://doi.org/10.1038/s41598-017-04041-9CrossRefGoogle ScholarPubMed
Kingston, HGM (2022) IL-17 and IL-17-producing cells in protection versus pathology. Nat Rev Immunol 23, 38–54 (2023). https://doi.org/10.1038/s41577-022-00746-9Google Scholar
Kwiatkowski, AJ, Stewart, JM, Cho, JJ, Avram, D, and Keselowsky, BG (2020) Nano and microparticle emerging strategies for treatment of autoimmune diseases: multiple sclerosis and type 1 diabetes. Advanced Healthcare Materials 9(11), 2000164. https://doi.org/10.1002/adhm.202000164CrossRefGoogle ScholarPubMed
Labib, DAA, Shaker, OG, and Elfarouk, LO (2016) Protective effects of nebivolol on acetic acid-induced ulcerative colitis in rats. Kasr Al Ainy Medical Journal 22(3), 99. DOI: 10.4103/1687-4625.195889.CrossRefGoogle Scholar
Langer, V, Vivi, E, Regensburger, D, Winkler, TH, Waldner, MJ, Rath, T, and Stürzl, M (2019) IFN-γ drives inflammatory bowel disease pathogenesis through VE-cadherin–directed vascular barrier disruption. The Journal of Clinical Investigation 129(11), 4691–4707. https://doi.org/10.1172/jci124884CrossRefGoogle ScholarPubMed
Lee, M and Chang, EB (2021) Inflammatory bowel diseases (IBD) and the microbiome-searching the crime scene for clues. Gastroenterology 160(2):524–537. doi: 10.1053/j.gastro.2020.09.056.CrossRefGoogle ScholarPubMed
Li, CW, Li, LL, Chen, S, Zhang, JX, and Lu, WL (2020) Antioxidant nanotherapies for the treatment of inflammatory diseases. Frontiers in Bioengineering and Biotechnology 8, 200. https://doi.org/10.3389/fbioe.2020.00200CrossRefGoogle ScholarPubMed
Li, Z, Li, D, Tsun, A, and Li, B (2015) FOXP3+ regulatory T cells and their functional regulation. Cellular & Molecular Immunology 12(5), 558–565. https://doi.org/10.1038/cmi.2015.10CrossRefGoogle ScholarPubMed
Lu, J, Dong, B, Chen, A, He, F, Peng, B, Wu, Z, and Li, W (2019) Escherichia coli promotes DSS‑induced murine colitis recovery through activation of the TLR4/NF‑κB signaling pathway‑. Molecular Medicine Reports 19(3), 2021–2028. https://doi.org/10.3892/mmr.2019.9848Google ScholarPubMed
Luzuriaga, MA, Welch, RP, Dharmarwardana, M, Benjamin, CE, Li, S, Shahrivarkevishahi, A, and Gassensmith, JJ (2019) Enhanced stability and controlled delivery of mof-encapsulated vaccines and their immunogenic response in vivo. ACS Applied Materials & Interfaces 11(10), 9740–9746. doi: 10.1021/acsami.8b20504CrossRefGoogle ScholarPubMed
Mazzachi, BC, Peake, MJ, and Ehrhardt, V (2000) Reference range and method comparison studies for enzymatic and Jaffe creatinine assays in plasma and serum and early morning urine. Clinical Laboratory 46(1-2): 53–55.Google ScholarPubMed
McDowell, C, Farooq, U, and Haseeb, M (2023) Inflammatory bowel disease. NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health. Stat Pearls [Internet]. Treasure Island (FL): StatPearls Publishing; Jan. https://www.ncbi.nlm.nih.gov/books/NBK470312/Google Scholar
Menachem, Y, Trop, S, Kolker, O, Shibolet, O, Alper, R, Nagler, A, and Ilan, Y (2005) Adoptive transfer of NK 1.1+ lymphocytes in immune-mediated colitis: a pro-inflammatory or a tolerizing subgroup of cells? Microbes and Infection 7(5-6), 825–835. https://doi.org/10.1016/j.micinf.2005.03.019CrossRefGoogle ScholarPubMed
Moreels, T, Nieuwendijk, R, De Man, J, Winter, D, Herman, A, Van Marck, E, and Pelckmans, P (2004) Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut 53(1), 99–107. https://doi.org/10.1016/j.micinf.2005.03.019CrossRefGoogle ScholarPubMed
Mostafa, EF, Metwally, A, and Hussein, AS (2018) Inflammatory bowel diseases prevalence in patients underwent colonoscopy in Zagazig University Hospitals. Afro-Egypt J Infect Endem Dis 8(2), 81–87 https://aeji.journals.ekb.eg/article_8740_ffbba6fe5569aaa27443e837ed936e7a.pdfGoogle Scholar
Na, SY and Moon, W (2019) Perspectives on current and novel treatments for inflammatory bowel disease. Gut and Liver 13(6), 604. https://doi.org/10.5009/gnl19019CrossRefGoogle ScholarPubMed
Negi, S, Saini, S, Tandel, N, Sahu, K, Mishra, RPN, and Tyagi, RK (2021) Translating Treg therapy for inflammatory bowel disease in humanized mice. Cells Jul 21;10(8),1847. doi: 10.3390/cells10081847. PMID: 34440615; PMCID: PMC8393385.CrossRefGoogle ScholarPubMed
Owusu, G, Obiri, DD, Ainooson, GK, Osafo, N, Antwi, AO, Duduyemi, BM, and Ansah, C (2020) Acetic acid-induced ulcerative colitis in Sprague Dawley rats is suppressed by hydroethanolic extract of Cordia vignei leaves through reduced serum levels of TNF-α and IL-6. International Journal of Chronic Diseases 6, 2020:8785497. https://doi.org/10.1155/2020/8785497Google Scholar
Pang, J, Ding, J, Zhang, L, Zhang, Y, Yang, Y, Bai, X, Liu, X, Jin, X, Guo, H, Yang, Y, and Liu, M (2020) Effect of recombinant serine protease from adult stage of Trichinella spiralis on TNBS-induced experimental colitis in mice. Int Immunopharmacol 86,106699. doi: 10.1016/j.intimp.2020.106699. Epub 2020 Jun 20. PMID: 32570037CrossRefGoogle Scholar
Patra, M, Mukherjee, R, Banik, M, Dutta, D, Begum, NA, and Basu, T (2017) Calcium phosphate-quercetin nanocomposite (CPQN): A multi-functional nanoparticle having pH indicating, highly fluorescent and anti-oxidant properties. Colloids Surf B Biointerfaces; 154, 63–73. doi: 10.1016/j.colsurfb.2017.03.018. Epub 2017 Mar 14. PMID: 28324689.CrossRefGoogle ScholarPubMed
Quijia, CR, Alves, RC, Hanck-Silva, G, GalvãoFrem, RC, Arroyos, G, and Chorilli, M (2022) Metal-organic frameworks for diagnosis and therapy of infectious diseases. Critical Reviews in Microbiology 48(2), 161–196. https://doi.org/10.1080/1040841x.2021.1950120CrossRefGoogle ScholarPubMed
Randhawa, P, Singh, K, Singh, N, and Jaggi, AS (2014) A review on chemical-induced inflammatory bowel disease models in rodents. The Korean Journal of Physiology & Pharmacology 18(4), 279–288. https://doi.org/10.4196/kjpp.2014.18.4.279CrossRefGoogle ScholarPubMed
Sarazin, A, Dendooven, A, Delbeke, M, Gatault, S, Pagny, A, Standaert, A, and Capron, M (2018) Treatment with P28GST, a schistosome-derived enzyme, after acute colitis induction in mice: decrease of intestinal inflammation associated with a down regulation of Th1/Th17 responses. PLoS One 13(12), e0209681. https://doi.org/10.1371/journal.pone.0209681CrossRefGoogle ScholarPubMed
Shaaban, NRA, El-Menshawy, SS, Salem, AE, and Othman, SSM (2021) Protective effects of propranolol and carvedilol on experimentally induced ulcerative colitis in male albino rat. European Journal of Molecular & Clinical Medicine 8(03), https://doi.org/10.13140/RG.2.2.22062.38724Google Scholar
Stidham, RW and Higgins, PD (2018) Colorectal cancer in inflammatory bowel disease. Clinics in Colon and Rectal Surgery 31(03), 168–178. doi: 10.1055/s-0037-1602237Google ScholarPubMed
Sun, XM, Guo, K, Hao, CY, Zhan, B, Huang, JJ, and Zhu, X (2019) Trichinella spiralis excretory–secretory products stimulate host regulatory T cell differentiation through activating dendritic cells. Cells 8 (11), 1404. doi: 10.3390/cells8111404CrossRefGoogle ScholarPubMed
Tee, JK, Ong, CN, Bay, BH, Ho, HK, and Leong, DT (2016) Oxidative stress by inorganic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol 8(3), 414–38. doi: 10.1002/wnan.1374. Epub 2015 Sep 10. PMID: 26359790CrossRefGoogle ScholarPubMed
Tietz, NW (2015) Tietz Fundamentals of Clinical Chemistry. 7th ed. pp 692 W.B. Elsevier Saunders, St. Louis.Google Scholar
Vakiti, RK, Garabato, BD, Schieber, NP, Rucks, MJ, Cao, Y, Webb, C, and Yan, B (2012) Synthesis and characterization of two-and three-dimensional calcium coordination polymers built with benzene-1, 3, 5-tricarboxylate and/or pyrazine-2-carboxylate. Crystal Growth & Design 12(8), 3937–3943. https://doi.org/10.1021/cg3003349CrossRefGoogle Scholar
Wang, L, Cui, J, Hu, DD, Liu, RD, and Wang, ZQ (2014) Identification of early diagnostic antigens from major excretory-secretory proteins of Trichinella spiralis muscle larvae using immunoproteomics. Parasites & Vectors 7(1), 1–8. https://doi.org/10.1186/1756-3305-7-40CrossRefGoogle ScholarPubMed
Xian, S, Lin, Y, Wang, H, and Li, J (2021) Calcium based metal–organic frameworks and their potential applications. Small 17(22), 2005165. https://doi.org/10.1002/smll.202005165CrossRefGoogle ScholarPubMed
Xie, X, Wu, Z, Wu, Y, Liu, J, Chen, X, Shi, X, and Tang, Z (2022) Cysteine protease of Clonorchis sinensis alleviates DSS-induced colitis in mice. PLOS Neglected Tropical Diseases 16(9), e0010774. https://doi.org/10.1371/journal.pntd.0010774CrossRefGoogle ScholarPubMed
Xu, J, Liu, M, Yu, P, Wu, L, and Lu, Y (2019) Effect of recombinant Trichinella spiralis cysteine proteinase inhibitor on TNBS-induced experimental inflammatory bowel disease in mice. International Immunopharmacology 66, 28–40. https://doi.org/10.1016/j.intimp.2018.10.043CrossRefGoogle ScholarPubMed
Yang, X, Yan, Y, Wang, Y, Zhan, B, Gu, Y, Cheng, Y, and Zhu, X (2014) Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice. PLoS One 9(5), e96454. https://doi.org/10.1371/journal.pone.0096454CrossRefGoogle ScholarPubMed
Yang, Y, Liu, L, Liu, X, Zhang, Y, Shi, H, Jia, W, and Bai, X (2020) Extracellular vesicles derived from Trichinella spiralis muscle larvae ameliorate TNBS-induced colitis in mice. Frontiers in Immunology 11, 1174. https://doi.org/10.3389/fimmu.2020.01174CrossRefGoogle ScholarPubMed
Yeshi, K, Ruscher, R, Hunter, L, Daly, NL, Loukas, A, and Wangchuk, P (2020) Revisiting inflammatory bowel disease: pathology, treatments, challenges and emerging therapeutics including drug leads from natural products. Journal of Clinical Medicine 9 (5), 1–39. doi: 10.3390/jcm9051273CrossRefGoogle ScholarPubMed
Young, DS (2001) Effects of Disease on Clinical Lab Tests. 4th Edition, AACC, Washington DC.Google Scholar
Zhu, L, Gu, P, and Shen, H (2019) Protective effects of berberine hydrochloride on DSS-induced ulcerative colitis in rats. International Immunopharmacology 68, 242–251. https://doi.org/10.1016/j.intimp.2018.12.036CrossRefGoogle ScholarPubMed