Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-20T03:26:40.544Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunolocalization and functional analysis of Opisthorchis viverrini-M60-like-1 metallopeptidase in animal models

Published online by Cambridge University Press:  21 April 2022

Woro D. Wendo ,
Sirikachorn Tangkawattana ,
Prasert Saichua ,
Binh T. T. Ta ,
Agatha R. K. Candra ,
Prasarn Tangkawattana  and
Sutas Suttiprapa Open the ORCID record for Sutas Suttiprapa [Opens in a new window]
Woro D. Wendo
Affiliation:
Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Graduate School, Khon Kaen University, Khon Kaen 40002, Thailand Department of Anatomy, Faculty of Veterinary Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia
Sirikachorn Tangkawattana*
Affiliation:
Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Tropical Disease Research Center, WHO Collaborating Centre for Research and Control of Opisthorchiasis, Khon Kaen University, Khon Kaen 40002, Thailand
Prasert Saichua
Affiliation:
Tropical Disease Research Center, WHO Collaborating Centre for Research and Control of Opisthorchiasis, Khon Kaen University, Khon Kaen 40002, Thailand Tropical Medicine Graduate Program, Academic Affairs, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Binh T. T. Ta*
Affiliation:
Tropical Medicine Graduate Program, Academic Affairs, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Agatha R. K. Candra
Affiliation:
Department of Biomedicine, School of Life Sciences, Indonesia International Institute for Life Sciences, Jakarta, Indonesia
Prasarn Tangkawattana
Affiliation:
Faculty of Veterinary Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
Sutas Suttiprapa*
Affiliation:
Tropical Disease Research Center, WHO Collaborating Centre for Research and Control of Opisthorchiasis, Khon Kaen University, Khon Kaen 40002, Thailand Tropical Medicine Graduate Program, Academic Affairs, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
*
Authors for correspondence: Sirikachorn Tangkawattana, E-mail: [email protected]; Sutas Suttiprapa, E-mail: [email protected]
Authors for correspondence: Sirikachorn Tangkawattana, E-mail: [email protected]; Sutas Suttiprapa, E-mail: [email protected]
Authors for correspondence: Sirikachorn Tangkawattana, E-mail: [email protected]; Sutas Suttiprapa, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Host mucins have crucial physical roles in preventing the parasitic establishment and maturation, and also in expelling the invading parasites. However, some parasites utilize mucinase enzymes to facilitate the infection. Recently, we have identified a mucinase enzyme of the liver fluke Opisthorchis viverrini, Ov-M60-like-1, which exhibits metallopeptidase activity against bovine submaxillary mucin substrate. Here, we aimed to study the localization of this enzyme in O. viverrini and the bile duct of hamsters using immunohistochemistry and functional analysis by mucin digestion in hamsters and mice tissues. The results showed that Ov-M60-like-1 was detected strongly in the tegument, tegumental cells, vitelline glands and mature eggs with miracidium. Expression in the gut, ovary and testis of the parasite was moderate while parenchyma showed slight colour intensity. In addition, the mucinase was also detected in the host biliary epithelial cells and goblet cells surrounding the worm. The mucinase assay revealed that the Ov-M60-like-1 could digest neutral mucin in the parenchyma, testis and seminal receptacle, but not the mucin in the tegument, tegumental cells and vitelline glands of the worm. The enzyme can also digest mucin in the cholangiocytes and modified the mixture type in the bile duct goblet cells of the infected hamsters, a susceptible host. In contrast, the enzyme was unable to digest neutral, acid and mixture mucin in the bile duct of the mice, a non-susceptible host. These findings indicate that Ov-M60-like-1 may have functions in both housekeeping tasks and host–parasite interactions, especially in modification of host susceptibility.

Keywords

ImmunolocalizationmetallopeptidasemucinmucinaseOpisthorchis viverriniOv-M60-like-1
Type
Research Article
Information
Parasitology , Volume 149 , Special Issue 10: Foodborne Trematodes – time to rise from neglected status , September 2022 , pp. 1356 - 1363
Check for updates
Copyright
Copyright © The Author(s), 2022. 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.)

References

Bancroft, J, Stevens, A and Tumer, D (1990) Theory and Practice of Histological Techniques, 3rd Edn. Edinburgh, UK: Churchill Livingstone Elsevier.Google Scholar
Chaiyadet, S, Smout, M, Johnson, M, Whitchurch, C, Turnbull, L, Kaewkes, S, Sotillo, J, Loukas, A and Sripa, B (2015) Excretory/secretory products of the carcinogenic liver fluke are endocytosed by human cholangiocytes and drive cell proliferation and IL6 production. International Journal for Parasitology 45, 773–781.CrossRefGoogle ScholarPubMed
Dalton, JP, Neill, SO, Stack, C, Collins, P, Walshe, A, Sekiya, M, Doyle, S, Mulcahy, G, Hoyle, D, Khaznadji, E, Moiré, N, Brennan, G, Mousley, A, Kreshchenko, N, Maule, AG and Donnelly, SM (2003) Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. International Journal for Parasitology 33, 1173–1181.CrossRefGoogle ScholarPubMed
de la Torre-Escudero, E, Gerlach, JQ, Bennett, APS, Cwiklinski, K, Jewhurst, HL, Huson, KM, Joshi, L, Kilcoyne, M, O'Neill, S, Dalton, JP and Robinson, MW (2019) Surface molecules of extracellular vesicles secreted by the helminth pathogen Fasciola hepatica direct their internalisation by host cells. PLoS Neglected Tropical Diseases 13, e0007087.CrossRefGoogle ScholarPubMed
Hasnain, SZ, McGuckin, MA, Grencis, RK and Thornton, DJ (2012) Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier. PLoS Neglected Tropical Diseases 6.CrossRefGoogle ScholarPubMed
Hasnain, SZ, Gallagher, AL, Grencis, RK and Thornton, DJ (2013) A new role for mucins in immunity: insights from gastrointestinal nematode infection. International Journal of Biochemistry & Cell Biology 45, 364–374.CrossRefGoogle ScholarPubMed
He, C and Ohnishi, K (2017) Efficient renaturation of inclusion body proteins denatured by SDS. Biochemical and Biophysical Research Communications 490, 1250–1253.CrossRefGoogle ScholarPubMed
Linden, S, Sutton, P, Karlsson, N, Korolik, V and McGuckin, M (2008) Mucins in the mucosal barrier to infection. Mucosal Immunology 1, 183–197.CrossRefGoogle ScholarPubMed
Lvova, MN, Tangkawattana, S, Balthaisong, S, Katokhin, AV, Mordvinov, VA and Sripa, B (2012) Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitology International 61, 167–172.CrossRefGoogle Scholar
Ninlawan, K, O'Hara, SP, Splinter, PL, Yongvanit, P, Kaewkes, S, Surapaitoon, A, LaRusso, NF and Sripa, B (2010) Opisthorchis viverrini excretory/secretory products induce Toll-like receptor 4 upregulation and production of interleukin 6 and 8 in cholangiocyte. Parasitology International 59, 616–621.CrossRefGoogle ScholarPubMed
Noach, I, Ficko-Blean, E, Pluvinage, B, Stuart, C, Jenkins, ML, Brochu, D, Buenbrazo, N, Wakarchuk, W, Burke, JE and Gilbert, M (2017) Recognition of protein-linked glycans as a determinant of peptidase activity. Proceedings of the National Academy of Sciences of the USA 114, E679–E688.CrossRefGoogle ScholarPubMed
Rizzardi, AE, Johnson, AT, Vogel, RI, Pambuccian, SE, Henriksen, J, Skubitz, AP, Metzger, GJ and Schmechel, SC (2012) Quantitative comparison of immunohistochemical staining measured by digital image analysis versus pathologist visual scoring. Diagnostic Pathology 7, 1–10.CrossRefGoogle ScholarPubMed
Suttiprapa, S, Mulvenna, J, Huong, NT, Pearson, MS, Brindley, PJ, Laha, T, Wongkham, S, Kaewkes, S, Sripa, B and Loukas, A (2009) Ov-APR-1, an aspartic protease from the carcinogenic liver fluke, Opisthorchis viverrini: functional expression, immunolocalization and subsite specificity. International Journal of Biochemistry & Cell Biology 41, 1148–1156.CrossRefGoogle ScholarPubMed
Suttiprapa, S, Sotillo, J, Smout, M, Suyapoh, W, Chaiyadet, S, Tripathi, T, Laha, T and Loukas, A (2018) Opisthorchis viverrini proteome and host–parasite interactions. Advances in Parasitology 102, 45–72.CrossRefGoogle ScholarPubMed
Ta, BT, Nguyen, DL, Jala, I, Dontumprai, R, Plumworasawat, S, Aighewi, O, Ong, E, Shawley, A, Potriquet, J, Saichua, P, van Diepen, A, Sripa, B, Hokke, CH and Suttiprapa, S (2020) Identification, recombinant protein production, and functional analysis of a M60-like metallopeptidase, secreted by the liver fluke Opisthorchis viverrini. Parasitology International 75, 102050.CrossRefGoogle ScholarPubMed
Tapader, R, Bose, D, Dutta, P, Das, S and Pal, A (2018) SslE (YghJ), a cell-associated and secreted lipoprotein of neonatal septicemic Escherichia coli, induces Toll-like receptor 2-dependent macrophage activation and proinflammation through NF-κB and MAP kinase signaling. Infection and Immunity 86, e00399-18.CrossRefGoogle ScholarPubMed
Theodoropoulos, G, Hicks, SJ, Corfield, AP, Miller, BG and Carrington, SD (2001) The role of mucins in host–parasite interactions: part II – helminth parasites. Trends in Parasitology 17, 130–135.CrossRefGoogle ScholarPubMed
Ueda, T, Mittal, AK, Fujimori, O and Yamada, K (1994) HID-AB2.5-PAS and HID-PAS methods for the histochemical analyses of a variety of carbohydrates. Okajimas Folia Anatomica Japonica 71, 51–57.CrossRefGoogle ScholarPubMed
Wattanavises, S, Silsirivanit, A, Sawanyawisuth, K, Cha'on, U, Waraasawapati, S, Saentaweesuk, W, Luang, S, Chalermwat, C, Wongkham, C and Wongkham, S (2019) Increase of MAL-II binding alpha2,3-sialylated glycan is associated with 5-FU resistance and short survival of cholangiocarcinoma patients. Medicina (Kaunas) 55, 761.CrossRefGoogle ScholarPubMed
Supplementary material: File

Wendo et al. supplementary material

Figure S1

Download Wendo et al. supplementary material(File)
File 1.4 MB