Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni

Lockyer, Anne E.; Spinks, Jenny; Kane, Richard A.; Hoffmann, Karl F.; Fitzpatrick, Jennifer M.; Rollinson, David; Noble, Leslie R.; Jones, Catherine S.

doi:10.1186/1471-2164-9-634

Cited by 69 publications

(77 citation statements)

References 79 publications

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“…The publicly available expression sequence data resulting from gene discovery efforts have been used to develop microarray platforms for more comprehensive study of the immune capabilities of B. glabrata toward pathogens (Adema et al, 2010; Hanington et al, 2010a, 2010b; Lockyer et al, 2008; 2012). Such approaches have revealed differences in the hemocyte responses to S. mansoni of susceptible and resistant B. glabrata , involving functional components and indicating possible regulatory pathways that have a role in effective immunity toward pathogens.…”

Section: From Snails To Genes and Immunitymentioning

confidence: 99%

Digenean-gastropod host associations inform on aspects of specific immunity in snails

Adema¹,

Loker²

2015

Developmental & Comparative Immunology

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Gastropod immunology is informed importantly by the study of the frequent encounters snails endure with digeneans (digenetic trematodes). One of the hallmarks of gastropod-digenean associations is their specificity: any particular digenean parasite species is transmitted by a limited subset of snail taxa. We discuss the nature of this specificity, including its immunological basis. We then review studies of the model gastropod Biomphalaria glabrata indicating that the baseline responses of snails to digeneans can be elevated in a specific manner. Studies incorporating molecular and functional approaches are then highlighted, and are further suggestive of the capacity for specific gastropod immune responses. These studies have led to the compatibility polymorphism hypothesis: the interactions between diversified fibrinogen-related proteins (FREPs) and diverse carbohydrate-decorated polymorphic parasite antigens determine recognition and trigger specific immunity. Complex glycan structures are also likely to play a role in the host specificity typifying snail-digenean interactions. We conclude by noting the dynamic and consequential interactions between snails and digeneans can be considered as drivers of diversification of digenean parasites and in the development and maintenance of specific immunity in gastropods.

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Section: From Snails To Genes and Immunitymentioning

confidence: 99%

Digenean-gastropod host associations inform on aspects of specific immunity in snails

Adema¹,

Loker²

2015

Developmental & Comparative Immunology

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“…Information on the expression of Hsps in adult freshwater gastropods seems limited to the pulmonate Biomphalaria glabrata (Lockyer et al, 2008) and to P. canaliculata (Zheng et al, 2012;present study). Hsp70 expression in embryonic or juvenile material is also known for these two species (Ittiprasert et al, 2009;Sun et al, 2010).…”

Section: Chaperone Protectionmentioning

confidence: 99%

Antioxidant and molecular chaperone defenses during estivation and arousal in the South American apple-snailPomacea canaliculata

Giraud-Billoud

Vega

Tosi

et al. 2012

Journal of Experimental Biology

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SUMMARYThe invasive Pomacea canaliculata estivates during periods of drought and should cope with harmful effects of reoxygenation during arousal. We studied thiobarbituric acid reactive substances (TBARS), enzymatic (superoxide dismutase, SOD and catalase, CAT) and non-enzymatic antioxidants (uric acid and reduced glutathione), and heat shock protein expression (Hsc70, Hsp70 and Hsp90) in (1) active control snails, (2) snails after 45days of estivation, and (3) aroused snails 20min and (4) 24h after water exposure, in midgut gland, kidney and foot. Both kidney and foot (but not the midgut gland) showed a TBARS increase during estivation and a decrease after arousal. Tissue SOD and CAT did not change in any experimental groups. Uric acid increased during estivation in all tissues, and it decreased after arousal in the kidney. Allantoin, the oxidation product of uric acid, remained constant in the midgut gland but it decreased in the kidney until 20min after arousal; however, allantoin levels rose in both kidney and foot 24h after arousal. Reduced glutathione decreased during estivation and arousal, in both midgut gland and kidney, and it remained constant in the foot. Hsc70 and Hsp70 kidney levels were stable during the activity-estivation cycle and Hsp90 expression decreases during estivation and recovers in the early arousal. In foot, the expression of Hsp70 and Hsp90 was high during activity and estivation periods and disminished after arousal. Results indicate that a panoply of antioxidant and molecular chaperone defences may be involved during the activity-estivation cycle in this freshwater gastropod.

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“…Lockyer et al (2004) demonstrated that production of HSP70 mRNA was up-regulated in schistosome-resistant B. glabrata mantle and brain tissue after in vivo S. mansoni infection using fluorescent-based differential display. The same researchers used a B. glabrata cDNA microarray to confirm that HSP70 mRNA expression was differentially up-regulated within 24 h in resistant S. mansoni-infected snails when compared to the susceptible strain (Lockyer et al 2008). In contrast, Ittiprasert et al (2009) demonstrated that juvenile susceptible B. glabrata exposed to S. mansoni miracidia for 24 h had increased HSP70 mRNA, but after 48 h expression levels decreased.…”

Section: Hsp70 Protein Reduction May Be Regulated By Effects Of Esps mentioning

confidence: 99%

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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Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni

Cited by 69 publications

References 79 publications

Digenean-gastropod host associations inform on aspects of specific immunity in snails

Digenean-gastropod host associations inform on aspects of specific immunity in snails

Antioxidant and molecular chaperone defenses during estivation and arousal in the South American apple-snailPomacea canaliculata

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

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