Transcriptome and Secretome Analysis of Intra-Mammalian Life-Stages of Calicophoron daubneyi Reveals Adaptation to a Unique Host Environment

Autor: R.E.B. Hanna, Kathryn M. Huson, Nicola A.M. Oliver, Philip Best, J.P. Barley, Sam Haldenby, Mark W. Robinson, Tom N. McNeilly, Steve Paterson, Erwan Atcheson, Yongxiang Fang
Rok vydání: 2021
Předmět:
α-CdE/S
anti–C. daubneyi excretory/secretory protein antibody
rumen fluke
Rumen
Host–pathogen interaction
AbD
antibody diluent
TCA
tricarboxylic acid
diagnostic
Virulence
Trematode Infections
Biochemistry
DE
differential expression
E/S
excretory/secretory
Analytical Chemistry
Microbiology
Transcriptome
Feces
03 medical and health sciences
TPM
transcripts per million
FaBP
fatty acid–binding protein
Cysteine Proteases
parasitic diseases
Animals
Helminths
Parasite hosting
HDM
helminth defense molecule
Paramphistomatidae
Molecular Biology
Pathogen
FA
formic acid
Secretome
030304 developmental biology
Life Cycle Stages
0303 health sciences
biology
Host (biology)
Research
Calicophoron daubneyi
030302 biochemistry & molecular biology
coproantigen
paramphistome
Helminth Proteins
biology.organism_classification
NEJ
newly excysted juvenile
Antigens
Helminth
emPAI
exponentially modified protein abundance index
ELISA
Cattle
Zdroj: Molecular & Cellular Proteomics : MCP
ISSN: 1535-9476
DOI: 10.1074/mcp.ra120.002175
Popis: Paramphistomosis, caused by the rumen fluke, Calicophoron daubneyi, is a parasitic infection of ruminant livestock, which has seen a rapid rise in prevalence throughout Western Europe in recent years. After ingestion of metacercariae (parasite cysts) by the mammalian host, newly excysted juveniles (NEJs) emerge and invade the duodenal submucosa, which causes significant pathology in heavy infections. The immature flukes then migrate upward, along the gastrointestinal tract, and enter the rumen where they mature and begin to produce eggs. Despite their emergence, and sporadic outbreaks of acute disease, we know little about the molecular mechanisms used by C. daubneyi to establish infection, acquire nutrients, and avoid the host immune response. Here, transcriptome analysis of four intramammalian life-cycle stages, integrated with secretome analysis of the NEJ and adult parasites (responsible for acute and chronic diseases, respectively), revealed how the expression and secretion of selected families of virulence factors and immunomodulators are regulated in accordance with fluke development and migration. Our data show that while a family of cathepsins B with varying S2 subsite residues (indicating distinct substrate specificities) is differentially secreted by NEJs and adult flukes, cathepsins L and F are secreted in low abundance by NEJs only. We found that C. daubneyi has an expanded family of aspartic peptidases, which is upregulated in adult worms, although they are under-represented in the secretome. The most abundant proteins in adult fluke secretions were helminth defense molecules that likely establish an immune environment permissive to fluke survival and/or neutralize pathogen-associated molecular patterns such as bacterial lipopolysaccharide in the microbiome-rich rumen. The distinct collection of molecules secreted by C. daubneyi allowed the development of the first coproantigen-based ELISA for paramphistomosis which, importantly, did not recognize antigens from other helminths commonly found as coinfections with rumen fluke.
Graphical abstract
Highlights • The first transcriptome data for intramammalian stages of Calicophoron daubneyi. • Comparative secretome profiles of infective stage and adult flukes. • New mechanistic insights into infectivity and pathogenicity. • Development of the first coproantigen-based ELISA for paramphistomosis.
In brief Paramphistomosis, caused by Calicophoron daubneyi, is a parasitic infection of ruminant livestock currently spreading throughout Western Europe. Here, transcriptome analysis of four intramammalian life-cycle stages, integrated with secretome profiling of the infective stage and adult parasites (responsible for acute and chronic diseases, respectively), revealed how selected families of unique virulence factors and immunomodulators are regulated in accordance with fluke development and migration. This analysis allowed the development of the first coproantigen-based ELISA for paramphistomosis.
Databáze: OpenAIRE
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