Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway

Zahoor, Zahida; Davies, Angela J.; Kirk, Ruth; Rollinson, David; Walker, Anthony J.

doi:10.1186/1756-3305-2-18

Cited by 36 publications

(35 citation statements)

References 43 publications

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“…In some experiments, the proteasome inhibitor Z-Leu-Leu-Leu-aldehyde (MG132; 50 μM; Merck Chemicals, Nottinghamshire, UK), the MEK1/2 inhibitor, 1,4-diamino-2,3-dicyano-1,4-bis[2-aminophenylthio]butadiene (U0126; 1-10 μM; Sigma), or vehicle control (0.1% (v/v) DMSO; Sigma) were added with or without ESPs. The inhibitor, U0126, has previously been used at these concentrations to block MEK1/2 activity in B. glabrata and Lymnaea stagnalis haemocytes, subsequently suppressing the phosphorylation (activation) of ERK (Plows et al 2004;Plows et al 2005;Wright et al 2006;Zahoor et al 2008Zahoor et al , 2009). The concentration chosen for MG132 was similar to that used by Kim et al (1999).…”

Section: Haemocytes and Haemocyte Treatmentsmentioning

confidence: 99%

“…After 30 min at room temperature (RT), the adherent haemocytes that formed the cell monolayer were washed twice with CBBS and then challenged for 1 h with S. mansoni ESPs. The ESP concentrations chosen (0-20 μg/ml in CBSS) were those employed in our previous studies (Zahoor et al 2008(Zahoor et al , 2009). In some experiments, the proteasome inhibitor Z-Leu-Leu-Leu-aldehyde (MG132; 50 μM; Merck Chemicals, Nottinghamshire, UK), the MEK1/2 inhibitor, 1,4-diamino-2,3-dicyano-1,4-bis[2-aminophenylthio]butadiene (U0126; 1-10 μM; Sigma), or vehicle control (0.1% (v/v) DMSO; Sigma) were added with or without ESPs.…”

Section: Haemocytes and Haemocyte Treatmentsmentioning

confidence: 99%

“…In vitro transformation of S. mansoni miracidia into mother sporocysts and collection of S. mansoni ESPs have been described previously (Zahoor et al 2008(Zahoor et al , 2009. Briefly, parasite eggs were isolated from the liver and spleen of S. mansoni-infected mice and left to hatch in spring water (Evian) for 3 h, before being collected, washed and concentrated using a Stericup HV filter unit with a 0.45 μm membrane (Millipore, Watford, UK).…”

Section: Collection Of S Mansoni Espsmentioning

confidence: 99%

“…ESPs from platyhelminths generally consist of antioxidant enzymes, protease inhibitors, cysteine proteases, small HSPs, glycolytic enzymes, mucins, calcium, ion-binding proteins and other unknown proteins (Connors et al 1991;Guillou et al 2007;Humphries and Yoshino 2008;Lodes and Yoshino 1989;Roger et al 2008;Wu et al 2009;Zelck and Von Janowsky 2004). These parasite-derived molecules can influence the behaviour of B. glabrata defence cells (haemocytes) by affecting their motility, adhesion, ability to phagocytose or encapsulate large antigens and produce reactive oxygen species and intracellular nitric oxide (NO; Connors et al 1991;Connors and Yoshino 1990;Humbert and Coustau 2001;Loker et al 1992;Lodes and Yoshino 1990;Zahoor et al 2009). Laboratory strains of B. glabrata exist that are either resistant or susceptible to S. mansoni infection; unlike in the susceptible strain, in the resistant strain the parasite is killed before it develops fully into a mother sporocyst.…”

Section: Introductionmentioning

confidence: 99%

“…These strains are therefore invaluable for studying snail-schistosome interactions in the context of parasite survival. Larval stage ESPs are thought to assist the survival of developing sporocysts in a susceptible snail host by interacting with haemocytes via cell surface receptors and modulating the activities of cell signalling pathways, such as the extracellular signal-regulated kinase (ERK) pathway that regulates cellular responses including cell spreading, NO and hydrogen peroxide production (Bayne 2009;Humphries and Yoshino 2008;Johnston and Yoshino 1996;Johnston and Yoshino 2001;Walker 2006;Zahoor et al 2008;Zahoor et al 2009). In the present study, we report for the first time that intracellular HSP70 protein levels in haemocytes from schistosome-susceptible and schistosomeresistant snails are reduced following exposure to S. mansoni larval ESPs.…”

Section: Introductionmentioning

confidence: 99%

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Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata

Zahoor

Davies²,

Kirk³

et al. 2010

Cell Stress and Chaperones

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Synthesis of heat shock proteins (HSPs) following cellular stress is a response shared by many organisms. Amongst the HSP family, the ∼70 kDa HSPs are the most evolutionarily conserved with intracellular chaperone and extracellular immunoregulatory functions. This study focused on the effects of larval excretory-secretory products (ESPs) from the parasite Schistosoma mansoni on HSP70 protein expression levels in haemocytes (defence cells) from its snail intermediate host Biomphalaria glabrata. S. mansoni larval stage ESPs are known to interfere with haemocyte physiology and behaviour. Haemocytes from two different B. glabrata strains, one which is susceptible to S. mansoni infection and one which is resistant, both showed reduced HSP70 protein levels following 1 h challenge with S. mansoni ESPs when compared to unchallenged controls; however, the reduction observed in the resistant strain was less marked. The decline in intracellular HSP70 protein persisted for at least 5 h in resistant snail haemocytes only. Furthermore, in schistosome-susceptible snails infected by S. mansoni for 35 days, haemocytes possessed approximately 70% less HSP70. The proteasome inhibitor, MG132, partially restored HSP70 protein levels in ESP-challenged haemocytes, demonstrating that the decrease in HSP70 was in part due to intracellular degradation. The extracellular signal-regulated kinase (ERK) signalling pathway appears to regulate HSP70 protein expression in these cells, as the mitogen-activated protein-ERK kinase 1/2 (MEK1/2) inhibitor, U0126, significantly reduced HSP70 protein levels. Disruption of intracellular HSP70 protein expression in B. glabrata haemocytes by S. mansoni ESPs may be a strategy employed by the parasite to manipulate the immune response of the intermediate snail host.

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Section: Haemocytes and Haemocyte Treatmentsmentioning

confidence: 99%

Section: Haemocytes and Haemocyte Treatmentsmentioning

confidence: 99%

Section: Collection Of S Mansoni Espsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata

Zahoor

Davies²,

Kirk³

et al. 2010

Cell Stress and Chaperones

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Localization of tyrosine hydroxylase‐like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis

Vallejo

Habib

Delgado

et al. 2014

J of Comparative Neurology

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Planorbid snails of the genus Biomphalaria are major intermediate hosts for the digenetic trematode parasite Schistosoma mansoni. Evidence suggests that levels of the neurotransmitter dopamine (DA) are reduced during the course of S. mansoni multiplication and transformation within the snail. This investigation used immunohistochemical methods to localize tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of catecholamines, in the nervous system of Biomphalaria. The two species examined, Biomphalaria glabrata and Biomphalaria alexandrina, are the major intermediate hosts for S. mansoni in sub-Saharan Africa, where more than 90% of global cases of human intestinal schistosomiasis occur. TH-like immunoreactive (THli) neurons were distributed throughout the central nervous system (CNS) and labeled fibers were present in all commissures, connectives, and nerves. Some asymmetries were observed, including a large distinctive neuron (LPeD1) in the pedal ganglion described previously in several pulmonates. The majority of TH-like immunoreactive neurons were detected in the peripheral nervous system (PNS), especially in lip and foot regions of the anterior integument. Independent observations supporting the dopaminergic phenotype of THli neurons included 1) block of LPeD1 synaptic signaling by the D2/3 antagonist sulpiride, and 2) the similar localization of aqueous aldehyde (FaGlu) induced fluorescence. The distribution of THli neurons indicates that, as in other gastropods, dopamine functions as a sensory neurotransmitter and in the regulation of feeding and reproductive behaviors in Biomphalaria. It is hypothesized that infection could stimulate transmitter release from dopaminergic sensory neurons and that dopaminergic signaling could contribute to modifications of both host and parasite behavior.

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Biomphalaria Snails and Larval Trematodes

Toledo

Fried

2011

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), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights.Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) v The history of research on the relationships between Biomphalaria spp. and larval trematodes, particularly Schistosoma mansoni, is long, active, and ongoing today. Snails of the genus Biomphalaria are of significant medical importance with many species living in freshwater habitats associated with human settlements; many of these snail species are obligate intermediate hosts of the human blood fluke S. mansoni, the causative agent of hepatosplenic schistosomiasis. This parasitic disease continues to disrupt the lives of about 200 million people in over 70 countries and prevents these individuals from otherwise reasonable expectations of healthy and productive lives. Furthermore, it is estimated that within the developing world, especially in sub-Saharan Africa, more than 700 million people are at risk of becoming infected, despite the efforts to control transmission in human and snail populations by mass chemotherapy and the use of molluscicides. Several factors, such as the absence of a schistosome vaccine, the recent appearance of resistance to antischistosome drugs, and human activities that expand snail habitats, have increased the need for a better understanding of schistosome-snail interactions. In recent years, the application of new technologies has contributed to the accumulation of considerable new information on this topic that may be of great use to biomedical scientists.In addition to the impact of Biomphalaria spp. on public health, these snails are also interesting models for the study of other topics such as population biology, including genetics and demography, proteomics, invertebrate immunobiology, mating systems, and biogeography, among others. Biomphalaria spp. snails have been extensively used as experimental biological models contributing significantly to new developments in many areas studied by biomedical scientists. Extensive coverage of these topics is included in this book, also considering trematode species other than schistosomes.The aim of the present book is to provide an overview of the recent advances in the Biomphalaria spp.-larval trematode interactions, especially in Biomphalariaschistosome systems. Emphasis is placed on gaps in our knowledge that must be filled to gain a better understanding of the relationships in these host-parasite systems. This may be critical for a deeper knowledge of the transmission of schistosomiasis and other snail-borne parasitic diseases. Pref...

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Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway

Cited by 36 publications

References 43 publications

Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata

Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata

Localization of tyrosine hydroxylase‐like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis

Biomphalaria Snails and Larval Trematodes

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