Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-29T14:12:25.536Z Has data issue: false hasContentIssue false
  • English
  • Français

Exploring the role of macrophages in determining the pathogenesis of liver fluke infection

Published online by Cambridge University Press:  27 May 2022

Susel Loli Quinteros ,
Bronwyn O'Brien  and
Sheila Donnelly Open the ORCID record for Sheila Donnelly [Opens in a new window]
Susel Loli Quinteros
Affiliation:
School of Life Sciences, Faculty of Science, The University of Technology Sydney, Ultimo, Australia
Bronwyn O'Brien
Affiliation:
School of Life Sciences, Faculty of Science, The University of Technology Sydney, Ultimo, Australia
Sheila Donnelly*
Affiliation:
School of Life Sciences, Faculty of Science, The University of Technology Sydney, Ultimo, Australia
*
Author for correspondence: Sheila Donnelly, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The food-borne trematodes, Opisthorchis viverrini and Clonorchis sinensis, are classified as group 1 biological carcinogens: definitive causes of cancer. By contrast, infections with Fasciola hepatica, also a food-borne trematode of the phylum Platyhelminthes, are not carcinogenic. This review explores the premise that the differential activation of macrophages during infection with these food-borne trematodes is a major determinant of the pathological outcome of infection. Like most helminths, the latter stages of infection with all 3 flukes induce M2 macrophages, a phenotype that mediates the functional repair of tissue damaged by the feeding and migratory activities of the parasites. However, there is a critical difference in how the development of pro-inflammatory M1 macrophages is regulated during infection with these parasites. While the activation of the M1 macrophage phenotype is largely suppressed during the early stages of infection with F. hepatica, M1 macrophages predominate in the bile ducts following infection with O. viverrini and C. sinensis. The anti-microbial factors released by M1 macrophages create an environment conducive to mutagenesis, and hence the initiation of tumour formation. Subsequently, the tissue remodelling processes induced by the M2 macrophages promote the proliferation of mutated cells, and the expansion of cancerous tissue. This review will also explore the interactions between macrophages and parasite-derived signals, and their contributions to the stark differences in the innate immune responses to infection with these parasites.

Keywords

CarcinogenesisClonorchis sinensisFasciola hepaticaimmunometabolismliver flukesmacrophagesOpisthorchis viverrini
Type
Review Article
Information
Parasitology , Volume 149 , Special Issue 10: Foodborne Trematodes – time to rise from neglected status , September 2022 , pp. 1364 - 1373
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

Aguayo, V, Valdés Fernandez, BN, Rodríguez-Valentín, M, Ruiz-Jiménez, C, Ramos-Benítez, MJ, Méndez, LB and Espino, AM (2019) Fasciola hepatica GST downregulates NF-κB pathway effectors and inflammatory cytokines while promoting survival in a mouse septic shock model. Scientific Reports 9, 2275.10.1038/s41598-018-37652-xCrossRefGoogle Scholar
Alvarado, R, To, J, Lund, ME, Pinar, A, Mansell, A, Robinson, MW, O'Brien, BA, Dalton, JP and Donnelly, S (2017) The immune modulatory peptide FhHDM-1 secreted by the helminth Fasciola hepatica prevents NLRP3 inflammasome activation by inhibiting endolysosomal acidification in macrophages. FASEB Journal 31, 85–95.10.1096/fj.201500093rCrossRefGoogle ScholarPubMed
Alvarez Rojas, CA, Ansell, BR, Hall, RS, Gasser, RB, Young, ND, Jex, AR and Scheerlinck, JP (2015) Transcriptional analysis identifies key genes involved in metabolism, fibrosis/tissue repair and the immune response against Fasciola hepatica in sheep liver. Parasites & Vectors 8, 124.10.1186/s13071-015-0715-7CrossRefGoogle ScholarPubMed
Andrejeva, G and Rathmell, JC (2017) Similarities and distinctions of cancer and immune metabolism in inflammation and tumors. Cell Metabolism 26, 49–70.10.1016/j.cmet.2017.06.004CrossRefGoogle ScholarPubMed
Andrews, S (1999) The life cycle of Fasciola hepatica. In Dalton, JP (ed.), Fasciolosis, 3rd Edn. Wallingford: CABI Publishing, pp. 1–29.Google Scholar
Attwood, HD and Chou, ST (1978) The longevity of Clonorchis sinensis. Pathology 10, 153–156.10.3109/00313027809063494CrossRefGoogle ScholarPubMed
Barron, L and Wynn, TA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. European Journal of Immunology 41, 2509–2514.10.1002/eji.201141869CrossRefGoogle ScholarPubMed
Bhamarapravati, N, Thammavit, W and Vajrasthira, S (1978) Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. The American Journal of Tropical Medicine and Hygiene 27, 787–794.10.4269/ajtmh.1978.27.787CrossRefGoogle ScholarPubMed
Bility, MT and Sripa, B (2014) Chronic Opisthorchis viverrini infection and associated hepatobiliary disease is associated with iron loaded M2-like macrophages. The Korean Journal of Parasitology 52, 695–699.10.3347/kjp.2014.52.6.695CrossRefGoogle ScholarPubMed
Biswas, SK, Gangi, L, Paul, S, Schioppa, T, Saccani, A, Sironi, M, Bottazzi, B, Doni, A, Vincenzo, B, Pasqualini, F, Vago, L, Nebuloni, M, Mantovani, A and Sica, A (2006) A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood 107, 2112–2122.10.1182/blood-2005-01-0428CrossRefGoogle ScholarPubMed
Chanmee, T, Ontong, P, Konno, K and Itano, N (2014) Tumor-associated macrophages as major players in the tumor microenvironment. Cancers 6, 1670–1690.CrossRefGoogle ScholarPubMed
Chen, S, Yang, J, Wei, Y and Wei, X (2020) Epigenetic regulation of macrophages: from homeostasis maintenance to host defense. Cellular & Molecular Immunology 17, 36–49.10.1038/s41423-019-0315-0CrossRefGoogle ScholarPubMed
Chen, X, Liu, Y, Gao, Y, Shou, S and Chai, Y (2021) The roles of macrophage polarization in the host immune response to sepsis. International Immunopharmacology 96, 107791.10.1016/j.intimp.2021.107791CrossRefGoogle ScholarPubMed
Cheng, N, Bai, X, Shu, Y, Ahmad, O and Shen, P (2020) Targeting tumor-associated macrophages as an antitumor strategy. Biochemical Pharmacology 183, 114354.CrossRefGoogle ScholarPubMed
Cliffe, LJ, Humphreys, NE, Lane, TE, Potten, CS, Booth, C and Grencis, RK (2005) Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science (New York, N.Y.) 308, 1463–1465.10.1126/science.1108661CrossRefGoogle ScholarPubMed
Coakley, G and Harris, NL (2020) Interactions between macrophages and helminths. Parasite Immunology 42, e12717.10.1111/pim.12717CrossRefGoogle ScholarPubMed
Colegio, OR, Chu, N-Q, Szabo, AL, Chu, T, Rhebergen, AM, Jairam, V, Cyrus, N, Brokowski, CE, Eisenbarth, SC and Phillips, GM (2014) Functional polarization of tumour associated macrophages by tumour-derived lactic acid. Nature 513, 559–563.CrossRefGoogle Scholar
Cortes-Selva, D and Fairfax, K (2021) Schistosome and intestinal helminth modulation of macrophage immunometabolism. Immunology 162, 123–134.10.1111/imm.13231CrossRefGoogle ScholarPubMed
Cortés, A, Muñoz-Antoli, C, Martín-Grau, C, Esteban, JG, Grencis, RK and Toledo, R (2015) Differential alterations in the small intestine epithelial cell turnover during acute and chronic infection with Echinostoma caproni (Trematoda). Parasites & Vectors 8, 334.CrossRefGoogle ScholarPubMed
Cox, N, Pokrovskii, M, Vicario, R and Geissmann, F (2021) Origins, biology, and diseases of tissue macrophages. Annual Review of Immunology 39, 313–344.CrossRefGoogle ScholarPubMed
Cwiklinski, K and Dalton, JP (2018) Advances in Fasciola hepatica research using ‘omics’ technologies. International Journal of Parasitology 48, 321–331.CrossRefGoogle ScholarPubMed
Cwiklinski, K, Dalton, JP, Dufresne, PJ, La Course, J, Williams, DJ, Hodgkinson, J and Paterson, S (2015) The Fasciola hepatica genome: gene duplication and polymorphism reveals adaptation to the host environment and the capacity for rapid evolution. Genome Biology 16, 71.CrossRefGoogle Scholar
Cwiklinski, K, Jewhurst, H, McVeigh, P, Barbour, T, Maule, AG, Tort, J, O'Neill, SM, Robinson, MW, Donnelly, S and Dalton, JP (2018) Infection by the helminth parasite Fasciola hepatica requires rapid regulation of metabolic, virulence, and invasive factors to adjust to its mammalian host. Molecular and Cellular Proteomics 17, 792–809.10.1074/mcp.RA117.000445CrossRefGoogle ScholarPubMed
de Martel, C, Ferlay, J, Franceschi, S, Vignat, J, Bray, F, Forman, D and Plummer, M (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. The Lancet Oncology 13, 607–615.10.1016/S1470-2045(12)70137-7CrossRefGoogle ScholarPubMed
Divangahi, M, Aaby, P, Khader, SA, Barreiro, LB, Bekkering, S, Chavakis, T, van Crevel, R, Curtis, N, DiNardo, AR, Dominguez-Andres, J, Duivenvoorden, R, Fanucchi, S, Fayad, Z, Fuchs, E, Hamon, M, Jeffrey, KL, Khan, N, Joosten, LAB, Kaufmann, E, Latz, E, Matarese, G, van der Meer, JWM, Mhlanga, M, Moorlag, SJCFM, Mulder, WJM, Naik, S, Novakovic, B, O'Neill, L, Ochando, J, Ozato, K, Riksen, NP, Sauerwein, R, Sherwood, ER, Schlitzer, A, Schultze, JL, Sieweke, MH, Benn, CS, Stunnenberg, H, Sun, J, van de Veerdonk, FL, Weis, S, Williams, DL, Xavier, R and Netea, MG (2021) Trained immunity, tolerance, priming and differentiation: distinct immunological processes. Nature Immunology 22, 2–6.10.1038/s41590-020-00845-6CrossRefGoogle ScholarPubMed
Donnelly, S, O'Neill, SM, Sekiya, M, Mulcahy, G and Dalton, JP (2005) Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infection and Immunity 73, 166–173.10.1128/IAI.73.1.166-173.2005CrossRefGoogle ScholarPubMed
Donnelly, S, O'Neill, SM, Stack, CM, Robinson, MW, Turnbull, L, Whitchurch, C and Dalton, JP (2010) Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3. Journal of Biological Chemistry 285, 3383–3392.CrossRefGoogle ScholarPubMed
Duan, Z and Luo, Y (2021) Targeting macrophages in cancer immunotherapy. Signal Transduction and Targeted Therapy 6, 127.CrossRefGoogle ScholarPubMed
Durbin, CG (1952) Longevity of the liver fluke, Fasciola sp. in sheep. In Otto, GF (ed.), Proceedings of the Helminthological Society of Washington. Washington, USA: The Helminthological Society of Washington, p. 120.Google Scholar
Fedorova, OS, Fedotova, MM, Zvonareva, OI, Mazeina, SV, Kovshirina, YV, Sokolova, TS, Golovach, EA, Kovshirina, AE, Konovalova, UV, Kolomeets, IL, Gutor, SS, Petrov, VA, Hattendorf, J, Ogorodova, LM and Odermatt, P (2020) Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Neglected Tropical Diseases 14, e0008421.CrossRefGoogle ScholarPubMed
Figueroa-Santiago, O and Espino, AM (2014) Fasciola hepatica fatty acid binding protein induces the alternative activation of human macrophages. Infection and Immunity 82, 5005–5012.CrossRefGoogle ScholarPubMed
Fried, B, Reddy, A and Mayer, D (2011) Helminths in human carcinogenesis. Cancer Letters 305, 239–249.CrossRefGoogle ScholarPubMed
Ghisletti, S, Barozzi, I, Mietton, F, Polletti, S, De Santa, F, Venturini, E, Gregory, L, Lonie, L, Chew, A, Wei, CL, Ragoussis, J and Natoli, G (2010) Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32, 317–328.10.1016/j.immuni.2010.02.008CrossRefGoogle ScholarPubMed
Ginhoux, F, Schultze, JL, Murray, PJ, Ochando, J and Biswas, SK (2016) New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nature Immunology 17, 34–40.CrossRefGoogle ScholarPubMed
Golden, O, Flynn, RJ, Read, C, Sekiya, M, Donnelly, SM, Stack, C, Dalton, JP and Mulcahy, G (2010) Protection of cattle against a natural infection of Fasciola hepatica by vaccination with recombinant cathepsin L1 (rFhCL1). Vaccine 28, 5551–5557.CrossRefGoogle ScholarPubMed
Guasconi, L, Chiapello, LS and Masih, DT (2015) Fasciola hepatica excretory–secretory products induce CD4+T cell anergy via selective up-regulation of PD-L2 expression on macrophages in a Dectin-1 dependent way. Immunobiology 220, 934–939.10.1016/j.imbio.2015.02.001CrossRefGoogle Scholar
Haswell-Elkins, MR, Mairiang, E, Mairiang, P, Chaiyakum, J, Chamadol, N, Loapaiboon, V, Sithithaworn, P and Elkins, DB (1994) Cross-sectional study of Opisthorchis viverrini infection and cholangiocarcinoma in communities within a high-risk area in northeast Thailand. International Journal of Cancer 59, 505–509.CrossRefGoogle ScholarPubMed
Helm, O, Held-Feindt, J, Grage-Griebenow, E, Reiling, N, Ungefroren, H, Vogel, I, Krüger, U, Becker, T, Ebsen, M and Röcken, C (2014) Tumor-associated macrophages exhibit pro and anti-inflammatory properties by which they impact on pancreatic tumorigenesis. International Journal of Cancer 135, 843–861.10.1002/ijc.28736CrossRefGoogle ScholarPubMed
Hesse, M, Modolell, M, La Flamme, AC, Schito, M, Fuentes, JM, Cheever, AW, Pearce, EJ and Wynn, TA (2001) Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of l-arginine metabolism. Journal of Immunology 167, 6533–6544.10.4049/jimmunol.167.11.6533CrossRefGoogle ScholarPubMed
Hongsrichan, N, Intuyod, K, Pinlaor, P, Khoontawad, J, Yongvanit, P, Wongkham, C, Roytrakul, S and Pinlaor, S (2014) Cytokine/chemokine secretion and proteomic identification of upregulated annexin A1 from peripheral blood mononuclear cells cocultured with the liver fluke Opisthorchis viverrini. Infection and Immunity 82, 2135–2147.10.1128/IAI.00901-13CrossRefGoogle ScholarPubMed
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Biological agents. Volume 100 B. A review of human carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 100(Pt B), pp. 1–441.Google Scholar
Ip, WE, Hoshi, N, Shouval, DS, Snapper, S and Medzhitov, R (2017) Anti-inflammatory effect of IL-10 mediated by metabolic reprogramming of macrophages. Science (New York, N.Y.) 356, 513–519.CrossRefGoogle ScholarPubMed
Kaewpitoon, N, Laha, T, Kaewkes, S, Yongvanit, P, Brindley, PJ, Loukas, A and Sripa, B (2008) Characterization of cysteine proteases from the carcinogenic liver fluke, Opisthorchis viverrini. Parasitology Research 102, 757–764.10.1007/s00436-007-0831-1CrossRefGoogle ScholarPubMed
Kang, JM, Bahk, YY, Cho, PY, Hong, SJ, Kim, TS, Sohn, WM and Na, BK (2010) A family of cathepsin F cysteine proteases of Clonorchis sinensis is the major secreted proteins that are expressed in the intestine of the parasite. Molecular and Biochemical Parasitology 170, 7–16.CrossRefGoogle ScholarPubMed
Kang, JM, Yoo, WG, Lê, HG, Lee, J, Sohn, WM and Na, BK (2020) Clonorchis sinensis MF6p/HDM (CsMF6p/HDM) induces pro-inflammatory immune response in RAW 264.7 macrophage cells via NF-κB-dependent MAPK pathways. Parasites & Vectors 13, 20.10.1186/s13071-020-3882-0CrossRefGoogle ScholarPubMed
Kaplan, RM (2001) Fasciola hepatica: a review of the economic impact in cattle and considerations for control. Veterinary Therapeutics: Research in Applied Veterinary Medicine 2, 40–50.Google ScholarPubMed
Kaya, M, Beştaş, R and Cetin, S (2011) Clinical presentation and management of Fasciola hepatica infection: single-center experience. World Journal of Gastroenterology 17, 4899–4904.CrossRefGoogle ScholarPubMed
Kieler, M, Hofmann, M and Schabbauer, G (2021) More than just protein building block: how amino acids and related metabolic pathways fuel macrophage polarization. The FEBS Journal 288, 3694–3714.CrossRefGoogle ScholarPubMed
Kim, JH, Choi, MH, Bae, YM, Oh, JK, Lim, MK and Hong, ST (2011) Correlation between discharged worms and fecal egg counts in human clonorchiasis. PLoS Neglected Tropical Diseases 5, e1339.CrossRefGoogle ScholarPubMed
Kim, EM, Kwak, YS, Yi, MH, Kim, JY, Sohn, WM and Yong, TS (2017) Clonorchis sinensis antigens alter hepatic macrophage polarization in vitro and in vivo. PLoS Neglected Tropical Diseases 11, e0005614.10.1371/journal.pntd.0005614CrossRefGoogle ScholarPubMed
Lalor, R, Cwiklinski, K, Calvani, N, Dorey, A, Hamon, S, Corrales, JL, Dalton, JP and De Marco Verissimo, C (2021) Pathogenicity and virulence of the liver flukes Fasciola hepatica and Fasciola gigantica that cause the zoonosis Fasciolosis. Virulence 12, 2839–2867.10.1080/21505594.2021.1996520CrossRefGoogle ScholarPubMed
Lavin, Y, Kobayashi, S, Leader, A, Amir, ED, Elefant, N, Bigenwald, C, Remark, R, Sweeney, R, Becker, CD, Levine, JH, Meinhof, K, Chow, A, Kim-Shulze, S, Wolf, A, Medaglia, C, Li, H, Rytlewski, JA, Emerson, RO, Solovyov, A, Greenbaum, BD, Sanders, C, Vignali, M, Beasley, MB, Flores, R, Gnjatic, S, Pe'er, D, Rahman, A, Amit, I and Merad, M (2017) Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses. Cell 169, 750–765.10.1016/j.cell.2017.04.014CrossRefGoogle ScholarPubMed
Lechner, A, Bohnacker, S and Esser-von Bieren, J (2021) Macrophage regulation & function in helminth infection. Seminars in Immunology 53, 101526.CrossRefGoogle ScholarPubMed
Lim, JH (2011) Liver flukes: the malady neglected. Korean Journal of Radiology 12, 269–279.10.3348/kjr.2011.12.3.269CrossRefGoogle ScholarPubMed
Liu, J, Geng, X, Hou, J and Wu, G (2021) New insights into M1/M2 macrophages: key modulators in cancer progression. Cancer Cell International 21, 389.CrossRefGoogle ScholarPubMed
Lu, XT, Gu, QY, Limpanont, Y, Song, LG, Wu, ZD, Okanurak, K and Lv, ZY (2018) Snail-borne parasitic diseases: an update on global epidemiological distribution, transmission interruption and control methods. Infectious Diseases of Poverty 7, 28.10.1186/s40249-018-0414-7CrossRefGoogle ScholarPubMed
Lund, ME, O'Brien, BA, Hutchinson, AT, Robinson, MW, Simpson, AM, Dalton, JP and Donnelly, S (2014) Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse. PLoS ONE 9, e86289.CrossRefGoogle ScholarPubMed
Machicado, C, Machicado, JD, Maco, V, Terashima, A and Marcos, LA (2016) Association of Fasciola hepatica infection with liver fibrosis, cirrhosis, and cancer: a systematic review. PLoS Neglected Tropical Diseases 10, e0004962.CrossRefGoogle ScholarPubMed
Machicado, C, Bertani, S, Herrera-Velit, P, Espinoza, J, Ruiz, E and Marcos, L (2018) Negative serology of Fasciola hepatica infection in patients with liver cancer in Peru: a preliminary report. Revista da Sociedade Brasileira de Medicina Tropical 51, 231–233.CrossRefGoogle Scholar
Martin, I, Cabán-Hernández, K, Figueroa-Santiago, O and Espino, AM (2015) Fasciola hepatica fatty acid binding protein inhibits TLR4 activation and suppresses the inflammatory cytokines induced by lipopolysaccharide in vitro and in vivo. Journal of Immunology 194, 3924–3936.10.4049/jimmunol.1401182CrossRefGoogle ScholarPubMed
Mas-Coma, S, Valero, MA and Bargues, MD (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Advances in Parasitology 69, 41–146.CrossRefGoogle ScholarPubMed
Mas-Coma, S, Valero, MA and Bargues, MD (2014) Fascioliasis. Advances in Experimental Medicine and Biology 766, 77–114.CrossRefGoogle ScholarPubMed
Mazzone, M, Menga, A and Castegna, A (2018) Metabolism and TAM functions – it takes two to tango. FEBS Journal 285, 700–716.CrossRefGoogle ScholarPubMed
Molina-Hernández, V, Mulcahy, G, Pérez, J, Martínez-Moreno, Á, Donnelly, S, O'Neill, SM, Dalton, JP and Cwiklinski, K (2015) Fasciola hepatica vaccine: we may not be there yet but we're on the right road. Veterinary Parasitology 208, 101–111.CrossRefGoogle Scholar
Mostafa, MH, Sheweita, SA and O'Connor, PJ (1999) Relationship between schistosomiasis and bladder cancer. Clinical Microbiology Reviews 12, 97–111.CrossRefGoogle ScholarPubMed
Mulvenna, J, Sripa, B, Brindley, PJ, Gorman, J, Jones, MK, Colgrave, ML, Jones, A, Nawaratna, S, Laha, T, Suttiprapa, S, Smout, MJ and Loukas, A (2010) The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics 10, 1063–1078.CrossRefGoogle ScholarPubMed
Murray, PJ (2017) Macrophage polarization. Annual Review of Physiology 79, 541–566.CrossRefGoogle ScholarPubMed
Murray, PJ, Allen, JE, Biswas, SK, Fisher, EA, Gilroy, DW, Goerdt, S, Gordon, S, Hamilton, JA, Ivashkiv, LB and Lawrence, T (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14–20.CrossRefGoogle ScholarPubMed
Netea, MG, Domínguez-Andrés, J, Barreiro, LB, Chavakis, T, Divangahi, M, Fuchs, E, Joosten, LAB, van der Meer, JWM, Mhlanga, MM, Mulder, WJM, Riksen, NP, Schlitzer, A, Schultze, JL, Stabell Benn, C, Sun, JC, Xavier, RJ and Latz, E (2020) Defining trained immunity and its role in health and disease. Nature Reviews Immunology 20, 375–388.10.1038/s41577-020-0285-6CrossRefGoogle ScholarPubMed
Nobs, SP and Kopf, M (2021) Tissue-resident macrophages: guardians of organ homeostasis. Trends in Immunology 42, 495–507.CrossRefGoogle ScholarPubMed
Noy, R and Pollard, JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41, 49–61.CrossRefGoogle ScholarPubMed
O'Neill, LA and Pearce, EJ (2016) Immunometabolism governs dendritic cell and macrophage function. The Journal of Experimental Medicine 213, 15–23.CrossRefGoogle ScholarPubMed
Palsson-Mcdermott, EM, Curtis, AM, Goel, G, Lauterbach, MA, Sheedy, FJ, Gleeson, LE, Van Den Bosch, MW, Quinn, SR, Domingo-Fernandez, R and Johnston, DG (2015) Pyruvate kinase M2 regulates Hif-1α activity and IL-1β induction and is a critical determinant of the Warburg effect in LPS-activated macrophages. Cell Metabolism 21, 65–80.CrossRefGoogle ScholarPubMed
Parisi, L, Gini, E, Baci, D, Tremolati, M, Fanuli, M, Bassani, B, Farronato, G, Bruno, A and Mortara, L (2018) Macrophage polarization in chronic inflammatory diseases: killers or builders? Journal of Immunology Research 2018, 8917804.10.1155/2018/8917804CrossRefGoogle ScholarPubMed
Pérez-Caballero, R, Buffoni, L, Martínez-Moreno, FJ, Zafra, R, Molina-Hernández, V, Pérez, J and Martínez-Moreno, Á (2018a) Expression of free radicals by peritoneal cells of sheep during the early stages of Fasciola hepatica infection. Parasites & Vectors 11, 500.CrossRefGoogle ScholarPubMed
Pérez-Caballero, R, Javier Martínez-Moreno, F, Zafra, R, Molina-Hernández, V, Pacheco, IL, Teresa Ruiz-Campillo, M, Escamilla, A, Pérez, J, Martínez-Moreno, Á and Buffoni, L (2018b) Comparative dynamics of peritoneal cell immunophenotypes in sheep during the early and late stages of the infection with Fasciola hepatica by flow cytometric analysis. Parasites & Vectors 11, 640.CrossRefGoogle ScholarPubMed
Perrigoue, JG, Marshall, FA and Artis, D (2008) On the hunt for helminths: innate immune cells in the recognition and response to helminth parasites. Cell Microbiology 10, 1757–1764.CrossRefGoogle Scholar
Piedrafita, D, Parsons, JC, Sandeman, RM, Wood, PR, Estuningsih, SE, Partoutomo, S and Spithill, TW (2001) Antibody-dependent cell-mediated cytotoxicity to newly excysted juvenile Fasciola hepatica in vitro is mediated by reactive nitrogen intermediates. Parasite Immunology 23, 473–482.10.1046/j.1365-3024.2001.00404.xCrossRefGoogle ScholarPubMed
Pinlaor, S, Ma, N, Hiraku, Y, Yongvanit, P, Semba, R, Oikawa, S, Murata, M, Sripa, B, Sithithaworn, P and Kawanishi, S (2004) Repeated infection with Opisthorchis viverrini induces accumulation of 8-nitroguanine and 8-oxo-7,8-dihydro-2′-deoxyguanine in the bile duct of hamsters via inducible nitric oxide synthase. Carcinogenesis 25, 1535–1542.10.1093/carcin/bgh157CrossRefGoogle Scholar
Pinlaor, S, Tada-Oikawa, S, Hiraku, Y, Pinlaor, P, Ma, N, Sithithaworn, P and Kawanishi, S (2005) Opisthorchis viverrini antigen induces the expression of toll-like receptor 2 in macrophage RAW cell line. International Journal of Parasitology 35, 591–596.CrossRefGoogle ScholarPubMed
Pinlaor, P, Kaewpitoon, N, Laha, T, Sripa, B, Kaewkes, S, Morales, ME, Mann, VH, Parriott, SK, Suttiprapa, S, Robinson, MW, To, J, Dalton, JP, Loukas, A and Brindley, PJ (2009) Cathepsin F cysteine protease of the human liver fluke, Opisthorchis viverrini. PLoS Neglected Tropical Diseases 3, e398.10.1371/journal.pntd.0000398CrossRefGoogle ScholarPubMed
Radostits, OM, Gay, CC, Hinchcliff, KW and Constable, P (eds) (2007) Veterinary Medicine: A Textbook of the Diseases of Cattle, Horses, Sheep and Pigs, 10th Edn. New York: Saunders/Elsevier.Google Scholar
Ramos-Benítez, MJ, Ruiz-Jiménez, C, Aguayo, V and Espino, AM (2017) Recombinant Fasciola hepatica fatty acid binding protein suppresses Toll-like receptor stimulation in response to multiple bacterial ligands. Scientific Reports 7, 5455.CrossRefGoogle ScholarPubMed
Ramsay, RJ, Sithithaworn, P, Prociv, P, Moorhouse, DE and Methaphat, C (1989) Density-dependent fecundity of Opisthorchis viverrini in humans, based on faecal recovery of flukes. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 241–242.CrossRefGoogle ScholarPubMed
Ravidà, A, Cwiklinski, K, Aldridge, AM, Clarke, P, Thompson, R, Gerlach, JQ, Kilcoyne, M, Hokke, CH, Dalton, JP and O'Neill, SM (2016) Fasciola hepatica surface tegument: glycoproteins at the interface of parasite and host. Molecular & Cellular Proteomics 15, 3139–315.CrossRefGoogle ScholarPubMed
Ray, D, Nelson, TA, Fu, CL, Patel, S, Gong, DN, Odegaard, JI and Hsieh, MH (2012) Transcriptional profiling of the bladder in urogenital schistosomiasis reveals pathways of inflammatory fibrosis and urothelial compromise. PLOS Neglected Tropical Diseases 6, e1912.CrossRefGoogle ScholarPubMed
Robinson, MW, Donnelly, S, Hutchinson, AT, To, J, Taylor, NL, Norton, RS, Perugini, MA and Dalton, JP (2011) A family of helminth molecules that modulate innate cell responses via molecular mimicry of host antimicrobial peptides. PLoS Pathogens 7, e1002042.CrossRefGoogle ScholarPubMed
Ruiz-Campillo, MT, Molina Hernandez, V, Escamilla, A, Stevenson, M, Perez, J, Martinez-Moreno, A, Donnelly, S, Dalton, JP and Cwiklinski, K (2017) Immune signatures of pathogenesis in the peritoneal compartment during early infection of sheep with Fasciola hepatica. Scientific Reports 7, 2782.CrossRefGoogle ScholarPubMed
Salmaninejad, A, Valilou, SF, Soltani, A, Ahmadi, S, Abarghan, YJ, Rosengren, RJ and Sahebkar, A (2019) Tumor-associated macrophages: role in cancer development and therapeutic implications. Cellular Oncology 42, 591–608.10.1007/s13402-019-00453-zCrossRefGoogle ScholarPubMed
Sanin, DE, Ge, Y, Marinkovic, E, Kabat, AM, Castoldi, A, Caputa, G, Grzes, KM, Curtis, JD, Willenborg, S, Dichtl, S, Reinhardt, S, Dahl, A, Pearse, EL, Eming, SA, Gerbaulet, A, Roers, A, Murray, PJ and Pearce, EJ (2021) Predictive framework of macrophage activation. bioRxiv 08.02.454825.Google Scholar
Shi, Y, Yu, K, Liang, A, Huang, Y, Ou, F, Wei, H, Wan, X, Yang, Y, Zhang, W and Jiang, Z (2020) Identification and analysis of the tegument protein and excretory–secretory products of the carcinogenic liver fluke Clonorchis sinensis. Frontiers in Microbiology 11, 555730.CrossRefGoogle ScholarPubMed
Shiels, J, Cwiklinski, K, Alvarado, R, Thivierge, K, Cotton, S, Gonzales Santana, B, To, J, Donnelly, S, Taggart, CC, Weldon, S and Dalton, JP (2020) Schistosoma mansoni immunomodulatory molecule Sm16/SPO-1/SmSLP is a member of the trematode-specific helminth defence molecules (HDMs). PLoS Neglected Tropical Diseases 14, e0008470.CrossRefGoogle ScholarPubMed
Sithithaworn, P, Sripa, B, Kaewkes, S, Nawa, Y and Haswell, MR (2014) Food-borne trematodes. In Farrar, J, Hotez, PJ, Junghanss, T, Kang, G, Lalloo, D and White, NJ (eds), Manson's Tropical Infectious Diseases, 23rd Edn. Philadelphia: Elsevier Saunders, pp. 726–736.CrossRefGoogle Scholar
Sripa, B and Kaewkes, S (2000) Localisation of parasite antigens and inflammatory responses in experimental opisthorchiasis. International Journal of Parasitology 30, 735–740.CrossRefGoogle ScholarPubMed
Sripa, B, Kaewkes, S, Intapan, PM, Maleewong, W and Brindley, PJ (2010) Food-borne trematodiases in Southeast Asia epidemiology, pathology, clinical manifestation and control. Advances in Parasitology 72, 305–350.CrossRefGoogle ScholarPubMed
Sripa, B, Jumnainsong, A, Tangkawattana, S and Haswell, MR (2018) Immune response to Opisthorchis viverrini infection and its role in pathology. Advances in Parasitology 102, 73–95.CrossRefGoogle Scholar
Steele, JA, Richter, CH, Echaubard, P, Saenna, P, Stout, V, Sithithaworn, P and Wilcox, BA (2018) Thinking beyond Opisthorchis viverrini for risk of cholangiocarcinoma in the lower Mekong region: a systematic review and meta-analysis. Infectious Diseases of Poverty 7, 44.CrossRefGoogle ScholarPubMed
Stempin, CC, Motrán, CC, Aoki, MP, Falcón, CR, Cerbán, FM and Cervi, L (2016) PD-L2 negatively regulates Th1-mediated immunopathology during Fasciola hepatica infection. Oncotarget 7, 77721–77731.CrossRefGoogle ScholarPubMed
Su, P, Wang, Q, Bi, E, Ma, X, Liu, L, Yang, M, Qian, J and Yi, Q (2020) Enhanced lipid accumulation and metabolism are required for the differentiation and activation of tumor-associated macrophages. American Association of Cancer Research 80, 1438–1450.CrossRefGoogle ScholarPubMed
Sulaiman, AA, Zolnierczyk, K, Japa, O, Owen, JP, Maddison, BC, Emes, RD, Hodgkinson, JE, Gough, KC and Flynn, RJ (2016) A trematode parasite derived growth factor binds and exerts influences on host immune functions via host cytokine receptor complexes. PLoS Pathogens 12, e1005991.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, 45–72.10.1016/bs.apar.2018.06.002CrossRefGoogle ScholarPubMed
Tao, J, Zhang, J, Ling, Y, Mccall, CE and Liu, TF (2018) Mitochondrial sirtuin 4 resolves immune tolerance in monocytes by rebalancing glycolysis and glucose oxidation homeostasis. Frontiers in Immunology 9, 419.CrossRefGoogle ScholarPubMed
Techasen, A, Loilome, W, Namwat, N, Duenngai, K, Cha'on, U, Thanan, R, Sithithaworn, P, Miwa, M and Yongvanit, P (2012) Opisthorchis viverrini-antigen induces expression of MARCKS during inflammation-associated cholangiocarcinogenesis. Parasitology International 61, 140–144.CrossRefGoogle ScholarPubMed
Thanee, M, Loilome, W, Techasen, A, Namwat, N, Boonmars, T, Pairojkul, C and Yongvanit, P (2015) Quantitative changes in tumor-associated M2 macrophages characterize cholangiocarcinoma and their association with metastasis. Asian Pacific Journal of Cancer Prevention 16, 3043–3050.CrossRefGoogle ScholarPubMed
Tliba, O, Sibille, P, Boulard, C and Chauvin, A (2000) Local hepatic immune response in rats during primary infection with Fasciola hepatica. Parasite 7, 9–18.CrossRefGoogle ScholarPubMed
Valero, MA, Navarro, M, Garcia-Bodelon, MA, Marcilla, A, Morales, M, Hernandez, JL, Mengual, P and Mas-Coma, S (2006) High risk of bacterobilia in advanced experimental chronic fasciolosis. Acta Tropica 100, 17–23.CrossRefGoogle ScholarPubMed
Valero, MA, Gironès, N, García-Bodelón, MA, Periago, MV, Chico-Calero, I, Khoubbane, M, Fresno, M and Mas-Coma, S (2008) Anaemia in advanced chronic fasciolosis. Acta Tropica 108, 35–43.CrossRefGoogle ScholarPubMed
Varga, T, Mounier, R, Horvath, A, Cuvellier, S, Dumont, F, Poliska, S, Ardjoune, H, Juban, G, Nagy, L and Chazaud, B (2016) Highly dynamic transcriptional signature of distinct macrophage subsets during sterile inflammation, resolution, and tissue repair. The Journal of Immunology 196, 4771–4782.10.4049/jimmunol.1502490CrossRefGoogle ScholarPubMed
Walsh, KP, Brady, MT, Finlay, CM, Boon, L and Mills, KH (2009) Infection with a helminth parasite attenuates autoimmunity through TGF-beta-mediated suppression of Th17 and Th1 responses. Journal of Immunology 183, 1577–1586.CrossRefGoogle ScholarPubMed
Wang, F, Zhang, S, Vuckovic, I, Jeon, R, Lerman, A, Folmes, C, Dzeja, PP and Herrmann, J (2018) Glycolytic stimulation is not a requirement for M2 macrophage differentiation. Cell Metabolism 28, 463–475.CrossRefGoogle Scholar
Wang, N, Bai, X, Jin, X, Tang, B, Yang, Y, Sun, Q, Li, S, Wang, C, Chang, Q, Liu, M and Liu, X (2021) The dynamics of select cellular responses and cytokine expression profiles in mice infected with juvenile Clonorchis sinensis. Acta Tropica 217, 105852.CrossRefGoogle ScholarPubMed
Wen, Y, Lambrecht, J, Ju, C and Tacke, F (2021) Hepatic macrophages in liver homeostasis and diseases-diversity, plasticity and therapeutic opportunities. Cellular & Molecular Immunology 18, 45–56.10.1038/s41423-020-00558-8CrossRefGoogle ScholarPubMed
Wu, J, Hayes, BW, Phoenix, C, Macias, GS, Miao, Y, Choi, HW, Hughes, FM Jr, Todd Purves, J, Lee Reinhardt, R and Abraham, SN (2020) A highly polarized TH2 bladder response to infection promotes epithelial repair at the expense of preventing new infections. Nature Immunology 21, 671–683.CrossRefGoogle ScholarPubMed
Wynn, TA, Cheever, AW, Jankovic, D, Poindexter, RW, Caspar, P, Lewis, FA and Sher, A (1995) An IL-12-based vaccination method for preventing fibrosis induced by schistosome infection. Nature 376, 594–596.CrossRefGoogle ScholarPubMed
Xie, M, Yu, Y, Kang, R, Zhu, S, Yang, L, Zeng, L, Sun, X, Yang, M, Billiar, TR and Wang, H (2016) Nature Communications 7, 13280.CrossRefGoogle Scholar
Yan, C, Wu, J, Xu, N, Li, J, Zhou, QY, Yang, HM, Cheng, XD, Liu, JX, Dong, X, Koda, S, Zhang, BB, Yu, Q, Chen, JX, Tang, RX and Zheng, KY (2021) TLR4 deficiency exacerbates biliary injuries and peribiliary fibrosis caused by Clonorchis sinensis in a resistant mouse strain. Frontiers in Cellular and Infection Microbiology 10, 526997.CrossRefGoogle Scholar
Zhao, A, Urban, JF Jr, Anthony, RM, Sun, R, Stiltz, J, van Rooijen, N, Wynn, TA, Gause, WC and Shea-Donohue, T (2008) Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135, 217–225.e1.CrossRefGoogle ScholarPubMed
Zhou, L, Shi, M, Zhao, L, Lin, Z, Tang, Z, Sun, H, Chen, T, Lv, Z, Xu, J, Huang, Y and Yu, X (2017) Clonorchis sinensis lysophospholipase A upregulates IL-25 expression in macrophages as a potential pathway to liver fibrosis. Parasites & Vectors 10, 295.CrossRefGoogle ScholarPubMed
Zhou, M, Wang, C, Lu, S, Xu, Y, Li, Z, Jiang, H and Ma, Y (2021) Tumor-associated macrophages in cholangiocarcinoma: complex interplay and potential therapeutic target. EBioMedicine 67, 103375.CrossRefGoogle ScholarPubMed