Host Immune response, Nutrition, and Metabolism in <i>Schistosoma</i> parasite-host Interactions
DOI:
https://doi.org/10.4314/njpar.v45i1.26Keywords:
Metabolism, Nutrition, Parasite-host interaction, Schistosomiasis, SchistosomaAbstract
Human schistosomiasis, a neglected tropical disease affecting millions of people, mainly in sub-Saharan Africa, is caused by a parasitic worm of the Schistosoma genus that resides in the veins of its host for many years. In parasite-host interactions, there is competition for survival between the parasite and its host because the parasite depends completely on the host for the maintenance of homeostasis. The host must protect itself from the harm caused by parasites in the process of obtaining food and shelter by attacking parasites with a strong immune defence system. Parasites have evolved strategies to survive in these unfavourable conditions created by the host. In this review, we examined the host immune response in Schistosoma parasite infection, the immune evasion mechanisms of Schistosoma parasites, nutrients, and the metabolic dependency of the parasite on the host.
References
Ezeh, C. O., Onyekwelu, K. C., Akinwale, O. P., Shan, L. and Wei, H. (2019). Urinary schistosomiasis in Nigeria: a 50 year review of prevalence, distribution and disease burden. Parasite, 26, 19.
Colley, D. G., Bustinduy, A. L., Secor, W. E. and King, C. H. (2014) Human schistosomiasis. Lancet, 383, 2253–2264.
Fishelson, Z., Amiri, P., Friend, D. S., Marikovsky, M., Petitt, M. and Newport, G. (1992). Schistosoma mansoni: Cellspecific expression and secretion of a serine protease during development of cercariae. Experimental Parasitology, 75(1):87–98.
Clerinx, J. and Gompel, A.V. (2011). Schistosomiasis in travellers and migrants. Travel Medicine and Infectious Disease, 9, 6–24.
doi: 10.1016/j.tmaid.2010.11.002
Doenhoff, M. J., Cioli, D. and Utzinger, J.(2008). Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases, 21, 659–667. doi: 10.1097/QCO.0b013e328318978f
Muller, R. (2002). Worms and Human Disease. 2nd ed. Wallingford, Oxon, UK: CABI Publishing.
King, C. L. (2001). Initiation and regulation of disease in schistosomiasis. In: Mahmoud AAF, editor. Schistosomiasis. London:Imperial College Press, pp. 213–264.
Matejuk, A. (2018). Skin immunity. Archivum Immunologiae et Therapiae Experimentali, 66: 45 – 54. doi:10.1007/s00005-017-0477-3
Mukai, K., Tsai, M., Starkl, P., Marichal, T. and Galli, S. J. (2026). IgE and mast cells in host defence against parasites and venoms. Seminars in Immunopathology, 38(5):581-603. doi: 10.1007/s00281-016-0565-1
Galli, S. J., Grimbaldeston, M. and Tsai, M. (2008). Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nature Reviews Immunology, 8:478–86. doi: 10.1038/nri2327
Zakeri, A., Hansen, E. P., Andersen, S. D., Williams, A. R. and Nejsum, P. (2018). Immunomodulation by helminths:intracellular pathways and extracellular vesicles. Frontiers in immunology, 9:2349. doi: 10.3389/fimmu.2018.02349
Ramaswamy, K., Kumar, P. and He, Y. X. (2000). A role for parasite-induced PGE2 in IL-10-mediated host immune regulation by skin stage schistosomula of Schistosoma mansoni. Journal of Immunology,165:4567–4574. doi: 10.4049/jimmunol.165.8.4567
Angeli, V., Faveeuw, C., Roye, O.,Fontaine, J., Teissier, E. and Capron, A.(2001). Role of the parasite-derivedprostaglandin D2 in the inhibition of
epidermal Langerhans cell migration during schistosomiasis infection. Journal ofExperimental Medicine, 193:1135–47. doi: 10.1084/jem.193.10.1135
Catto, B. A., Lewis, F. A. and Ottesen, E. A. (1980). Cercaria-induced histamine release: a factor in the pathogenesis of schistosome
dermatitis? American Journal of Tropical Medicine and Hygiene, 29:886–889. doi: 10.4269/ajtmh.1980.29.886
El-Ridi, R., Mohamed, S. H. and Tallima, H. (2003). Incubation of Schistosoma mansoni lung-stage schistosomula in corn oil exposes their surface membrane antigenic specificities. Journal of Parasitology, 89, 1064–1077. doi: 10.1645/GE-3122RN
Goldring, O. L., Clegg, J. A., Smithers, S. R. and Terry, R. J. (1976). Acquisition of human blood group antigens by Schistosoma mansoni. Clinical and Experimental Immunology, 26:181–187.
Horta, M. F., Ramalho-Pinto, F. J. and Fatima, M. (1991). Role of human decayaccelerating factor in the evasion of Schistosoma mansonifrom the complementmediated killing in vitro. Journal of Experimental Medicine, 174, 1399–1406. doi: 10.1084/jem.174.6.1399
Hambrook, J. R. and Hanington, P. C. (2021). Immune evasion strategies of schistosomes. Frontiers in immunology, 4; 11: 624178.
doi: 10.3389/fimmu.2020.624178
Mebius, M. M., van Genderen, P. J., Urbanus, R. T., Tielens, A. G., de Groot, P. G. and van Hellemond, J. J. (2013). Interference with the host haemostatic system by schistosomes. PLOS Pathogens, 9, e1003781. doi: 10.1371/journal.ppat.1003781
Gader, A. G. M. A. (2009). Tissue factor pathway inhibitor (TFPI): A natural coagulation inhibitor and potential therapeutic agent - A review. Journal of Taibah University Medical Sciences, 4, 1–15.
Ranasinghe, S. L., Fischer, K., Gobert, G. N. and McManus, D. P. (2015). Functional expression of a novel Kunitz type protease inhibitor from the human blood fluke Schistosoma mansoni. Parasites & Vectors,8, 1–10.
Mebius, M. M., van Genderen, P. J., Urbanus, R. T., Tielens, A. G., and de Groot, P. G. (2013). Interference with the host haemostatic system by schistosomes. PLOS Pathogens, 9:e1003781. doi: 10.1371/journal.ppat.1003781
Ramajo-Hernandez, A., Perez-Sanchez, R., Ramajo-Martin, V. and Oleaga, A. (2007). Schistosoma bovis: plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Experimental Parasitology, 115, 83–91. Doi: 10.1016/j.exppara.2006.07.003
Wang, Q., Da’dara, A. A. and Skelly, P. J. (2017). The human blood parasite Schistosomamans oni expresses extracellular tegumental calpains that cleave the blood clotting protein fibronectin.Scientific Reports, 7(1):1–13. doi: https://doi.org/10.1038/s41598-017-13141-5
Pearce, E. J., Hall, B. F. and Sher, A.(1990). Host-specific evasion of the alternative complement pathway by schistosomes correlates with the presence of a phospholipase c-sensitive surface molecular resembling human decay accelerating factor. Journal of Immunology, 144, 2751–2756.
Horn, M., Fajtová, P., Arreola, L.R., Ulrychová, L., Bartošová-Sojková, P. and Franta, Z. (2014). Trypsin - and chymotrypsin-like serine proteases in Schistosoma mansoni –‘the undiscovered country. PLoS Neglected Tropical Diseases, 8:e2766. doi: 10.1371/journal.pntd.0002766
Quezada, L. A. L., Sajid, M., Lim, K. C. and McKerrow, J. H. (2012). Ablood fluke serine protease inhibitor regulates an endogenous larval elastase. Journal of Biological Chemistry 287:7074–7083. doi: 10.1074/jbc.M111.313304
Levy-Holtzman, R. and Schechter, I.(1994). Schistosome extracts with heat shock factor activity revealed by the gel shift assay. Parasitology, 108,35–42. doi:10.1017/s0031182000078495
Hockley, D. J. and McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegumental during development from cercaria to adult worm. International Journal of Parasitology, 3,13– 25. Doi: 10.1016/0020-7519(73)90004-0
McLaren, D. J. and Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, 269: 147–149. doi: https://doi.org/10.1038/269147a0
Lienhard, G. E., Slot, J. W., James, D. E. and Mueckler, M. M. (1992). How cells absorb glucose. Scientific American, 266, 86–91. doi: 10.1038/scientificamerican0192-86
Skelly, P. J., Kim, J. W., Cunningham, J., and Shoemaker, C. B. (1994). Cloning, characterization, and functional expression of cDNAs encoding glucose transporter proteins from the human parasite Schistosoma mansoni. Journal of Biological Chemistry, 269, 4247–4253.
Skelly, P. J. and Shoemaker, C. B. (1996). Rapid appearance and asymmetric distribution of glucose transporter SGTP4 at the apical surface of intramammalian stage Schistosoma mansoni. Proceedings of the National Academy of Sciences of the United States of America, 93, 3642–3646. doi: 10.1073/pnas.93.8.3642
Zhong, C., Skelly, P. J., Leaffer, D., Cohn, R. G., Caulfield, J. P. and Shoemaker, C. B.(1995). Immunolocalization of a Schistosoma mansoni facilitated diffusion glucose transporter to the basal, but not the apical, membranes of the surface syncytium. Parasitology, 110(4), 383–394. doi:
1017/s0031182000064726
Beuding, E. (1950). Carbohydrate metabolism of Schistosoma mamansoni. Journal of General Physiology, 33,475–495. doi: 10.1085/jgp.33.5.475
Rogers, W. P. (1947). Histological distribution of alkaline phosphatase in helminth parasites.Nature, 159, 374-375.
Robinson, O. L. H.(1961). Phosphatases in Schistoso mamansoni. Nature, 191, 473-474.
Fripp, P. (1967). The sites of (1-14C) glucose assimilation in Schistosomahaematobium. Comparative Biochemistry and Physiology, 23(3), 893–898.
Senft, A. W. (1976). Observations on the physiology of the gut of Schistosoma mansoni. In: Bossche HVd, editor. The biochemistry of parasites and host parasite relationships. Oxford: North-HollandPublishing Co. pp. 335
Tort, J., Brindley, P. J., Knox, D., Wolfe, K. H. and Dalton, J. P. (1999). Proteinases and associated genes of parasitic helminths. Advances in Parasitology, 43: 161–266. doi: 10.1016/s0065-308x(08)60243-2
McCarthy, E., Stack, C., Donnelly, S. M., Doyle, S., and Mann, V. H. (2004). Leucine amino peptidase of the human blood flukes, Schistosoma mansoni and Schistosomajaponicum. International Journal forParasitology , 34: 703–714. doi:10.1016/j.ijpara.2004.01.008
Furlong, S. T. (1991). Unique roles for lipids in Schistosoma mansoni. Parasitology Today, 7: 59-62. doi: 10.1016/0169-4758(91)90192-q
Brouwers, J. F., Smeenk, I. M. B., van Golde, L. M. G., and Tielens, A. G. M. (1997). The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni. Molecular and Biochemical Parasitology, 88, 175 - 85. Doi: 10.1016/s0166-6851(97)00091-1
Rogers, M. V. (1991). Do parasites express receptors for host lipoproteins? Parasitology Today, 7: 117-120. doi: 10.1016/0169-4758(91)90170-s
Rumjanek, F. D., Campos, E. G. and Alonso, L. C. C. (1988). Evidence for the occurrence of LDL receptors in the extracts of schistosomula of Schistosoma mansoni. Molecular and Biochemical Parasitology, 28: 145-152.
Tempone, A. J., Bianconi, M. L. and Rumjanek, F. D. (1997). Interaction of human LDL with the tegument of adult Schistosoma mansoni. Molecular and Cellular Biochemistry, 177, 139–144. doi: 10.1023/a:1006801216344
Michiel, L. B., Mirjam, M. M., Martin, H., Jos, F. B., Aloysius, G.M. and Tielens J. H.(2018). Schistosoma mansoni does not and cannot oxidize fatty acids, but these are used for biosynthetic purposes instead.International Journal for Parasitology, 463984. doi: 10.1016/j.ijpara.2019.03.005
Molehin, A. J. (2020). Schistosomiasis vaccine development: update on human clinical trials. Journal of BiomedicalScience, 27, 28. doi: 10.1186/s12929-020-0621-y
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. doi: 10.3389/fimmu.2020.01821
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Nigerian Journal of Parasitology
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
