Influence of Trichobilharzia regenti (Digenea: Schistosomatidae) on the defence activity of Radix lagotis (Lymnaeidae) Haemocytes
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25372492
PubMed Central
PMC4221104
DOI
10.1371/journal.pone.0111696
PII: PONE-D-14-29981
Knihovny.cz E-zdroje
- MeSH
- extracelulárním signálem regulované MAP kinasy metabolismus MeSH
- fagocytóza imunologie MeSH
- hemocyty imunologie metabolismus parazitologie MeSH
- interakce hostitele a parazita imunologie MeSH
- Lymnaea imunologie metabolismus parazitologie MeSH
- peroxid vodíku metabolismus MeSH
- proteinkinasa C metabolismus MeSH
- Schistosomatidae * ultrastruktura MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- extracelulárním signálem regulované MAP kinasy MeSH
- peroxid vodíku MeSH
- proteinkinasa C MeSH
Radix lagotis is an intermediate snail host of the nasal bird schistosome Trichobilharzia regenti. Changes in defence responses in infected snails that might be related to host-parasite compatibility are not known. This study therefore aimed to characterize R. lagotis haemocyte defence mechanisms and determine the extent to which they are modulated by T. regenti. Histological observations of R. lagotis infected with T. regenti revealed that early phases of infection were accompanied by haemocyte accumulation around the developing larvae 2-36 h post exposure (p.e.) to the parasite. At later time points, 44-92 h p.e., no haemocytes were observed around T. regenti. Additionally, microtubular aggregates likely corresponding to phagocytosed ciliary plates of T. regenti miracidia were observed within haemocytes by use of transmission electron microscopy. When the infection was in the patent phase, haemocyte phagocytic activity and hydrogen peroxide production were significantly reduced in infected R. lagotis when compared to uninfected counterparts, whereas haemocyte abundance increased in infected snails. At a molecular level, protein kinase C (PKC) and extracellular-signal regulated kinase (ERK) were found to play an important role in regulating these defence reactions in R. lagotis. Moreover, haemocytes from snails with patent infection displayed lower PKC and ERK activity in cell adhesion assays when compared to those from uninfected snails, which may therefore be related to the reduced defence activities of these cells. These data provide the first integrated insight into the immunobiology of R. lagotis and demonstrate modulation of haemocyte-mediated responses in patent T. regenti infected snails. Given that immunomodulation occurs during patency, interference of snail-host defence by T. regenti might be important for the sustained production and/or release of infective cercariae.
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Van der Knaap WPW, Adema CM, Sminia T (1993) Invertebrate blood cells: morphological and functional aspects of the haemocytes in the pond snail Lymnaea stagnalis . Comp Haematol Int 3: 20–26.
Adema CM, Hertel LA, Miller RD, Loker ES (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci U S A 94: 8691–8696. PubMed PMC
Loker ES, Bayne CJ, Buckley PM, Kruse KT (1982) Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by haemocytes of juveniles of the 10-R2 strain of Biomphalaria glabrata . J Parasitol 68: 84–94. PubMed
Hahn UK, Bender RC, Bayne CJ (2001) Killing of Schistosoma mansoni sporocysts by haemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87: 292–299. PubMed
Adema CM, van Deutekom-Mulder EC, Van der Knaap WPW, Meuleman EA, Sminia T (1991) Generation of oxygen radicals in haemocytes of the snail Lymnaea stagnalis in relation to the rate of phagocytosis. Dev Comp Immunol 15: 17–26. PubMed
Ito T, Matsutani T, Mori K, Nomura T (1992) Phagocytosis and hydrogen peroxide production by phagocytes of the sea urchin Strongylocentrotus nudus . Dev Comp Immunol 16: 287–294. PubMed
Plows LD, Cook RT, Davies AJ, Walker AJ (2004) Activation of extracellular-signal regulated kinase is required for phagocytosis by Lymnaea stagnalis haemocytes. Biochim Biophys Acta 1692: 25–33. PubMed
Plows LD, Cook RT, Davies AJ, Walker AJ (2005) Carbohydrates that mimic schistosome surface coat components affect ERK and PKC signalling in Lymnaea stagnalis haemocytes. Int J Parasitol 35: 293–302. PubMed
Lacchini AH, Davies AJ, Mackintosh D, Walker AJ (2006) Beta-1, 3-glucan modulates PKC signalling in Lymnaea stagnalis defence cells: a role for PKC in H2O2 production and downstream ERK activation. J Exp Biol 209: 4829–4840. PubMed
Humphries JE, Yoshino TP (2008) Regulation of hydrogen peroxide release in circulating hemocytes of the planorbid snail Biomphalaria glabrata . Dev Comp Immunol 32: 554–562. PubMed PMC
Plows LD, Cook RT, Davies AJ, Walker AJ (2006) Phagocytosis by Lymnaea stagnalis haemocytes: A potential role for phosphatidylinositol 3-kinase but not protein kinase A. J Invertebr Pathol 91: 74–77. PubMed
Zelck UE, Gege BE, Schmid S (2007) Specific inhibitors of mitogen activated protein kinase and PI3-K pathways impair immune responses by haemocytes of trematode intermediate host snails. Dev Comp Immunol 31: 321–331. PubMed
Noda S, Loker ES (1989) Phagocytic activity of hemocytes of M-line Biomphalaria glabrata snails: effect of exposure to the trematode Echinostoma paraensei . J Parasitol 75: 261–269. PubMed
Dikkeboom R, Van der Knaap WPW, Van den Bovenkamp W, Tijnagel JM, Bayne CJ (1988) The production of toxic oxygen metabolites by hemocytes of different snail species. Dev Comp Immunol 12: 509–520. PubMed
Gorbushin AM, Iakovleva NV (2008) The enigma of the haemogram left-shift in periwinkles infected with trematodes. Fish Shellfish Immunol 24: 745–751. PubMed
Walker AJ (2006) Do trematode parasites disrupt defence-cell signalling in their snail host? Trends Parasitol 22: 154–159. PubMed
Zahoor Z, Davies AJ, Kirk RS, Rollinson D, Walker AJ (2008) Disruption of ERK signalling in Biomphalaria glabrata defence cells by Schistosoma mansoni: implications for parasite survival in the snail host. Dev Comp Immunol 32: 1561–1571. PubMed
Horák P, Kolářová L, Dvořák J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5: 349–357. PubMed
Huňová K, Kašný M, Hampl V, Leontovyč R, Kuběna A, et al. (2012) Radix spp.: Identification of trematode intermediate hosts in the Czech Republic. Acta Parasitol 57: 273–284. PubMed
Kolářová L, Horák P, Skírnisson K, Marečková H, Doenhoff M (2013) Cercarial dermatitis, a neglected allergic disease. Clin Rev Allergy Immunol 45: 63–74. PubMed
Horák P, Adema CM, Kolářová L (2002) Biology of the schistosome genus Trichobilharzia . Adv Parasitol 52: 155–233. PubMed
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208–212. PubMed PMC
Sminia T (1972) Structure and function of blood and connective tissue cells of the fresh water pulmonate Lymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Z Zellforsch Mikrosk Anat 130: 497–526. PubMed
Bender RC, Broderick EJ, Goodall CP, Bayne CJ (2005) Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. J Parasitol 91: 275–279. PubMed
Arumugam M, Romestand B, Torreilles J, Roch P (2000) In vitro production of superoxide and nitric oxide (as nitrite and nitrate) by Mytilus galloprovincialis haemocytes upon incubation with PMA or laminarin or during yeast phagocytosis. Eur J Cell Biol 79: 513–519. PubMed
Lehmacher W, Wassmer G (1999) Adaptive sample size calculations in group sequential trials. Biometrics 55: 1286–1290. PubMed
Walker AJ, Plows LD (2003) Bacterial lipopolysaccharide modulates Protein Kinase C signalling in Lymnaea stagnalis hemocytes. Biol Cell 95: 527–533. PubMed
Mohamed AH, Sharaf El-Din AT, Mohamed AM, Habib MR (2011) Tissue response exhibited by Biomphalaria alexandrina snails from different Egyptian localities following Schistosoma mansoni exposure. Exp Parasitol 127: 789–794. PubMed
Bayne CJ, Buckley PM, DeWan PC (1980) Macrophagelike hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro . J Parasitol 66: 413–419. PubMed
Bayne CJ, Buckley PM, DeWan PC (1980) Schistosoma mansoni: cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata . Exp Parasitol 50: 409–416. PubMed
Nacif-Pimenta R, de Mattos ACA, Orfano AS, Barbosa L, Pimenta PFP, et al. (2012) Schistosoma mansoni in susceptible and resistant snail strains Biomphalaria tenagophila: in vivo tissue response and in vitro hemocyte interactions. PloS One 7: 1–12. PubMed PMC
Amen RI, Baggen JMC, Bezemer PD, de Jong-Brink MD (1992) Modulation of the activity of the internal defence system of the pond snail Lymnaea stagnalis by the avian schistosome Trichobilharzia ocellata . Parasitol 104: 33–40. PubMed
de Jong-Brink MD, Bergamin-Sassen M, Soto M (2001) Multiple strategies of schistosomes to meet their requirements in the intermediate snail host. Parasitol 123: 129–141. PubMed
Lie KJ, Jeong KH, Heyneman D (1981) Selective interference with granulocyte function induced by Echinostoma paraensei (Trematoda) larvae in Biomphalaria glabrata (Mollusca). J Parasitol 67: 790–796. PubMed
Adema CM, Arguello DF, Stricker SA, Loker ES (1994) A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa . J Parasitol 80: 719–727. PubMed
Théron A, Pages JR, Rognon A (1997) Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes. Exp Parasitol 85: 1–9. PubMed
Mitta G, Adema CM, Gourbal B, Loker ES, Théron A (2012) Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev Comp Immunol 37: 1–8. PubMed PMC
Abou-El-Naga IF, Radwan EH (2012) Defense response of susceptible and resistant Biomphalaria alexandrina snails against Schistosoma mansoni infection. Rev Biol Trop 60: 1195–1204. PubMed
Suresh PG, Reju MK, Mohandas A (1994) Factors influencing total haemocyte counts in freshwater gastropods. Comp Haematol Int 4: 17–24.
Flye-Sainte-Marie J, Soudant P, Lambert C, Le Goic N, Goncalvez M, et al. (2009) Variability of the hemocyte parameters of Ruditapes philippinarum in the field during an annual cycle. J Exp Mar Biol Ecol 377: 1–11.
Mounkassa JB, Jourdane J (1990) Dynamics of the leukocytic response of Biomphalaria glabrata during the larval development of Schistosoma mansoni and Echinostoma liei . J Invertebr Pathol 55: 306–311. PubMed
Loker ES, Cimino DF, Stryker GA, Hertel LA (1987) The effect of size of M line Biomphalaria glabrata on the course of development of Echinostoma paraensei . J Parasitol 73: 1090–1098. PubMed
Riley EM, Chappell LH (1992) Effect of infection with Diplostomum spathaceum on the internal defense system of Lymnaea stagnalis . J Invertebr Pathol 59: 190–196.
Nunez PE, Adema CM, de Jong-Brink MD (1994) Modulation of the bacterial clearance activity of haemocytes from the freshwater mollusc, Lymnaea stagnalis, by the avian schistosome, Trichobilharzia ocellata . Parasitol 109: 299–310. PubMed
Connors VA, Yoshino TP (1990) In vitro effect of larval Schistosoma mansoni excretory-secretory products on phagocytosis-stimulated superoxide production in hemocytes from Biomphalaria glabrata . J Parasitol 76: 895–902. PubMed
Iakovleva NV, Shaposhnikova TG, Gorbushin AM (2006) Rediae of echinostomatid and heterophyid trematodes suppress phagocytosis of haemocytes in Littorina littorea (Gastropoda: Prosobranchia). Exp Parasitol 113: 24–29. PubMed
Humphries JE, Yoshino TP (2003) Cellular receptors and signal transduction in molluscan hemocytes: connections with the innate immune system of vertebrates. Integr Comp Biol 43: 305–312. PubMed
García-García E, Prado-Álvarez M, Novoa B, Figueras A, Rosales C (2008) Immune responses of mussel hemocyte subpopulations are differentially regulated by enzymes of the PI 3-K, PKC, and ERK kinase families. Dev Comp Immunol 32: 637–653. PubMed
Schwartz MA (2001) Integrin signaling revisited. Trends Cell Biol 11: 466–470. PubMed
Chen Q, Lin TH, Der CJ, Juliano RL (1996) Integrin-mediated activation of MEK and mitogen-activated protein kinase is independent of Ras. J Biol Chem 271: 18122–18127. PubMed
Hampton MB, Kettle AJ, Winterbourn CC (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007–3017. PubMed
Impact of trematode infections on periphyton grazing rates of freshwater snails