Identification and functional characterization of Oncomelania hupensis macrophage migration inhibitory factor involved in the snail host innate immune response to the parasite Schistosoma japonicum

Huang, Shuaiqin; Cao, Yunchao; Lu, Minghua; Peng, Wenfeng; Lin, Jiaojiao; Tang, Chongti; Tang, Liang

doi:10.1016/j.ijpara.2017.01.005

Cited by 20 publications

(13 citation statements)

References 78 publications

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“…Previous phylogenetic studies on MIF/D-DT (D-DT now also often referred to as MIF-2 [68]) in metazoans were either restricted to specific taxonomic groups such as insects [18], arthropods [69], or mollusks [70], or were focused on the relation between sequences from a single species and known sequences from vertebrates [14]. Several of these phylogenies supported a classification of MIF and D-DT variants from metazoans [13,71]. The present extended cross-kingdom analysis shows that MIF sequences from most metazoan phyla, such as nematodes, insects, or mollusks, do not form monophyletic groups.…”

Section: Discussionmentioning

confidence: 99%

“…For example, in the gastropod snail, Biomphalaria glabrata , MIF contributes to the activation of immune responses, promotes immune cell proliferation, and inhibits p53-mediated apoptosis [12]. These functions seem to be general features of MIF in mollusks [13], but also occur in invertebrates such as crustaceans and echinoderms [14]. Even more intriguing were the findings that plants possess MIF genes (named MDL for MIF/DDT-like) [15], and that aphids secrete a MIF protein upon feeding to manipulate plant immunity [16].…”

Section: Introductionmentioning

confidence: 99%

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Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily

Michelet

Danchin

Jaouannet

et al. 2019

Genes

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Macrophage migration inhibitory factors (MIF) are multifunctional proteins regulating major processes in mammals, including activation of innate immune responses. MIF proteins also play a role in innate immunity of invertebrate organisms or serve as virulence factors in parasitic organisms, raising the question of their evolutionary history. We performed a broad survey of MIF presence or absence and evolutionary relationships across 803 species of plants, fungi, protists, and animals, and explored a potential relation with the taxonomic status, the ecology, and the lifestyle of individual species. We show that MIF evolutionary history in eukaryotes is complex, involving probable ancestral duplications, multiple gene losses and recent clade-specific re-duplications. Intriguingly, MIFs seem to be essential and highly conserved with many sites under purifying selection in some kingdoms (e.g., plants), while in other kingdoms they appear more dispensable (e.g., in fungi) or present in several diverged variants (e.g., insects, nematodes), suggesting potential neofunctionalizations within the protein superfamily.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily

Michelet

Danchin

Jaouannet

et al. 2019

Genes

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“…RNAi-mediated knockdown confirmed immune function of B. glabrata MIF, yielding increased parasite burden following exposure to S. mansoni (Baeza-Garcia et al, 2010). Likewise, in Oncomelania hupensis a more distantly related prosobranch gastropod, expression of MIF increased after challenge with Schistosoma japonicum and its involvement in the activation, differentiation and recruitment of hemocytes was demonstrated: RNAi knockdown of MIF decreased the proportion of phagocytic circulating hemocytes and restrains the migration of blood cells from the host towards the site of infection (Huang et al, 2017).…”

Section: Elevated Representation Of Immune-related Molecules In Resistant Snailsmentioning

confidence: 71%

Natural resistance to Fasciola hepatica (Trematoda) in Pseudosuccinea columella snails: A review from literature and insights from comparative “omic” analyses

Alba

Tetreau

Chaparro

et al. 2019

Developmental & Comparative Immunology

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The snail Pseudosuccinea columella is one of the main vectors of the medically-important trematode Fasciola hepatica. In Cuba, the existence of natural P. columella populations that are either susceptible or resistant to F. hepatica infection offers a unique snail-parasite for study of parasite-host compatibility and immune function in gastropods. Here, we review all previous literature on this system and present new "omic" data that provide a molecular baseline of both P. columella phenotypes from naïve snails. Comparison of whole snail transcriptomes (RNAseq) and the proteomes of the albumen gland (2Delectrophoresis, MS) revealed that resistant and susceptible strains differed mainly in an enrichment of particular biological processes/functions and a greater abundance of proteins/transcripts associated with immune defense/stress response in resistant snails. These results indicate a differential allocation of molecular resources to self-maintenance and survival in resistant P. columella that may cause enhanced responsiveness to stressors (i.e. F. hepatica infection or tolerance to variations in environmental pH/total water hardness), possibly as trade-off against reproduction and the ecological cost of resistance previously suggested in resistant populations of P. columella. Highlights► Comparative "omic" analyses of P. columella offer clues for resistance to F. hepatica. ► Naïve resistant snails display a higher molecular competence for defense/stress responses. ► Constitutively broad expression of immune factors associates with resistance to F. hepatica. ► Overrepresented pH/osmotic regulators endorse the pH tolerance of resistant snails. ► Resource allocation to defense/stress response endorse reproductive trade-offs.Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.

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“…Huang et al found that found that OhMIF displays significantly increased expression in snails following challenge with S. japonicum. Furthermore, Knockdown of OhMIF significantly reduced the percentage of phagocytic cell populations in circulating hemocytes [32]. Lately, Zhao et al [33] identified 16 Toll-like receptors (TLRs) in O. hupensis.…”

Section: Discussionmentioning

confidence: 99%

Temporal transcriptome change of Oncomelania hupensis revealed by Schistosoma japonicum invasion

et al. 2020

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Background: The freshwater snail Oncomelania hupensis is the obligate intermediate host for Schistosoma japonicum in China. Transcriptomic examination of snail-schistosome interactions can provide valuable information of host response at physiological and immune levels. Methods: To investigate S. japonicum-induced changes in O. hupensis gene expression, we utilized high-throughput sequencing to identify transcripts that were differentially expressed between infected snails and their uninfected controls at two key time-point, Day 7 and Day 30 after challenge. Time-series transcriptomic profiles were analyzed using R package DESeq 2, followed by GO, KEGG and (weighted gene correlation network analysis) WGCNA analysis to elucidate and identify important molecular mechanism, and subsequently understand host-parasite relationship. The identified unigenes was verified by bioinformatics and real-time PCR. Possible adaptation molecular mechanisms of O. hupensis to S. japonicum challenge were proposed. Results: Transcriptomic analyses of O. hupensis by S. japonicum invasion yielded billion reads including 92,144 annotated transcripts. Over 5000 differentially expressed genes (DEGs) were identified by pairwise comparisons of infected libraries from two time points to uninfected libraries in O. hupensis. In total, 6032 gene ontology terms and 149 KEGG pathways were enriched. After the snails were infected with S. japonicum on Day 7 and Day 30, DEGs were shown to be involved in many key processes associated with biological regulation and innate immunity pathways. Gene expression patterns differed after exposure to S. japonicum. Using WGCNA, 16 modules were identified. Module-trait analysis identified that a module involved in RNA binding, ribosome, translation, mRNA processing, and structural constituent of ribosome were strongly associated with S. japonicum invasion. Many of the genes from enriched KEGG pathways were involved in lysosome, spliceosome and ribosome, indicating that S. japonicum invasion may activate the regulation of ribosomes and immune response to infection in O. hupensis. Conclusions: Our analysis provided a temporally dynamic gene expression pattern of O. hupensis by S. japonicum invasion. The identification of gene candidates serves as a foundation for future investigations of S. japonicum infection. Additionally, major DEGs expression patterns and putative key regulatory pathways would provide useful information to construct gene regulatory networks between host-parasite crosstalk.

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Identification and functional characterization of Oncomelania hupensis macrophage migration inhibitory factor involved in the snail host innate immune response to the parasite Schistosoma japonicum

Cited by 20 publications

References 78 publications

Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily

Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily

Natural resistance to Fasciola hepatica (Trematoda) in Pseudosuccinea columella snails: A review from literature and insights from comparative “omic” analyses

Temporal transcriptome change of Oncomelania hupensis revealed by Schistosoma japonicum invasion

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