Gene expression analysis distinguishes tissue-specific and gender-related functions among adult Ascaris suum tissues

Abstract

Over a billion people are infected by Ascaris spp. intestinal parasites. To clarify functional differences among tissues of adult A. suum, we compared gene expression by various tissues of these worms by expression microarray methods.. The A. suum genome was sequenced and assembled to allow generation of microarray elements. Expression of over 40,000 60-mer elements was investigated in a variety of tissues from both male and female adult worms. Nearly 50 percent of the elements for which signal was detected exhibited differential expression among different tissues. The unique profile of transcripts identified for each tissue clarified functional distinctions among tissues, such as chitin binding in the ovary and peptidase activity in the intestines. Interestingly, hundreds of gender-specific elements were characterized in multiple nonreproductive tissues of female or male worms, with most prominence of gender differences in intestinal tissue. A. suum genes from the same family were frequently expressed differently among tissues. Transcript abundance for genes specific to A. suum, by comparison to Caenorhabditis elegans, varied to a greater extent among tissues than for genes conserved between A. suum and C. elegans. Analysis using C. elegans protein interaction data identified functional modules conserved between these two nematodes, resulting in identification of functional predictions of essential subnetworks of protein interactions and how these networks may vary among nematode tissues. A notable finding was very high module similarity between adult reproductive tissues and intestine. Our results provide the most comprehensive assessment of gene expression among tissues of a parasitic nematode to date.

Genome-Wide Tissue-Specific Gene Expression, Co-expression and Regulation of Co-expressed Genes in Adult Nematode Ascaris suum

“…This term was identified as being enriched in the head of A. suum in the previous microarray study [16], and was enriched only in the head-overexpressed genes in this study, which could be expected since most of the other internal tissues are not cuticle-lined, or are only partially lined with cuticle (e.g. pharynx or the distal posterior part of the intestine-anus).…”

Molecular mechanism of serine/threonine protein phosphatase 1 (PP1cα–PP1r7) in spermatogenesis of Toxocara canis

“…Tissue transcriptional studies of some important genes have been reported in A. suum, H. contortus and B. malayi, which have provided valuable information regarding tissue-specific genes (Yin et al, 2008;Wang et al, 2013;Rosa et al, 2014). For example, Bm-shp-1 expression in the epithelium of uterine and Bm-msp-1 in spermatocytes and spermatids indicated potential roles in reproductive processes (Jiang et al, 2008).…”

“…Recent molecular investigations have provided invaluable data of gender-specific or -enriched genes in development and reproductive processes that could be potential targets to disrupt development or reproduction of parasites (Nisbet and Gasser, 2004;Nisbet et al, 2008;Li et al, 2011;Wang et al, 2013). Specifically, the functional roles of the male-specific serine/threonine protein phosphatase 1 (PP1) gene (stp-1) in reproduction have been investigated in Oesophagostomum dentatum (Boag et al, 2000;Boag et al, 2003), Trichostrongylus vitrinus, Haemonchus contortus and T. canis (Hu et al, 2007;Campbell et al, 2010;Ma et al, 2014), indicating potential roles of stp-1 in spermatogenesis of nematodes.…”

Functional and Phylogenetic Characterization of Proteins Detected in Various Nematode Intestinal Compartments*

“…A previous gene expression study in A. suum (14) found that the intestine expressed many more gender-specific genes (and had many more gender-specific functions) than other somatic tissues tested; (2) NHR-25, which is expressed in the C. elegans intestine and regulates an endocrine signaling cascade that ultimately modulates dietary fat uptake and de novo fat synthesis (83); (3) CEH-30, an anti-apoptotic gene regulating sexual identity and is transcriptionally repressed by TRA-1 in C. elegans (84) (the TF for the most significantly enriched motif in the intestinal tissue); (4) ELT-1, and (5) ELT-3, which are functionally redundant GATA transcription factors responsible for early intestine development in C. elegans (85), but only ELT-3 has been implicated in controlling the expression of age-related genes in the intestine (86).…”

“…However, the parasitic roundworm Ascaris suum (size 15-40 cm; which also has a complete draft genome available (12,13)) is large enough that the intestine can be physically manipulated for this purpose. The large size of the A. suum intestine has also supported the broad molecular characterization of intestinal cell functions based on gene expression studies using expressed sequence tags (3), microarray (14) and RNA-seq approaches (15). These studies analyzed the transcript expression level in whole intestinal tissue relative to other tissues but not protein expression or compartmentalization of proteins within intestinal tissue, although a proteomic study of A. suum proteins in nonintestinal fluids including perienteric and uterine fluids was recently reported (16).…”