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Infection with the gastrointestinal nematode Ostertagia ostertagi in cattle affects mucus biosynthesis in the abomasum.

Rinaldi M, Dreesen L, Hoorens PR, Li RW, Claerebout E, Goddeeris B, Vercruysse J, Van Den Broek W, Geldhof P - Vet. Res. (2011)

Bottom Line: Several genes involved in mucin core structure synthesis, branching and oligomerization, such as GCNT3, GCNT4, A4GNT and protein disulphide isomerases were found to be upregulated.Finally, transcription levels of 2 trefoil factors, TFF1 and TFF3, which are co-expressed with mucins in the GI tract, were also found to be significantly upregulated in infected animals.Although the alterations in mucus biosynthesis started early during infection, the biggest effects were found when adult worms were present on the surface of the abomasal mucosa and are likely caused by the alterations in mucosal cell populations, characterized by hyperplasia of mucus secreting cells.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium. peter.geldhof@UGent.be.

ABSTRACT
The mucus layer in the gastrointestinal (GI) tract is considered to be the first line of defense to the external environment. Alteration in mucus components has been reported to occur during intestinal nematode infection in ruminants, but the role of mucus in response to abomasal parasites remains largely unclear. The aim of the current study was to analyze the effects of an Ostertagia ostertagi infection on the abomasal mucus biosynthesis in cattle. Increased gene expression of MUC1, MUC6 and MUC20 was observed, while MUC5AC did not change during infection. Qualitative changes of mucins, related to sugar composition, were also observed. AB-PAS and HID-AB stainings highlighted a decrease in neutral and an increase in acidic mucins, throughout the infection. Several genes involved in mucin core structure synthesis, branching and oligomerization, such as GCNT3, GCNT4, A4GNT and protein disulphide isomerases were found to be upregulated. Increase in mucin fucosylation was observed using the lectin UEA-I and through the evaluation of fucosyltransferases gene expression levels. Finally, transcription levels of 2 trefoil factors, TFF1 and TFF3, which are co-expressed with mucins in the GI tract, were also found to be significantly upregulated in infected animals. Although the alterations in mucus biosynthesis started early during infection, the biggest effects were found when adult worms were present on the surface of the abomasal mucosa and are likely caused by the alterations in mucosal cell populations, characterized by hyperplasia of mucus secreting cells.

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Histochemical staining of Carnoy's fixed, paraffin-embedded abomasum sections of Holstein cows after Ostertagia ostertagi infection. PAS (A-D) stained mucins in pink; AB-PAS pH 2.5 (E-H) stained neutral mucins in magenta and acidic mucins in blue; HID-AB (I-N) stained sialylated mucins in blue and sulphated mucins in brown. (A, E, I) negative control, (B, F, L) infected for 14 days, (C, G, M) infected for 21 days, (D, H, N) exposed for 60 days. Original magnification 10×.
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Figure 1: Histochemical staining of Carnoy's fixed, paraffin-embedded abomasum sections of Holstein cows after Ostertagia ostertagi infection. PAS (A-D) stained mucins in pink; AB-PAS pH 2.5 (E-H) stained neutral mucins in magenta and acidic mucins in blue; HID-AB (I-N) stained sialylated mucins in blue and sulphated mucins in brown. (A, E, I) negative control, (B, F, L) infected for 14 days, (C, G, M) infected for 21 days, (D, H, N) exposed for 60 days. Original magnification 10×.

Mentions: Histochemistry was performed to detect mucins in the mucosa of the abomasum during an infection with O. ostertagi (Figure 1). PAS, which stains all glycoproteins including mucins, was observed in surface mucus cells (SMCs) and mucus neck cells (MNCs) of uninfected animals (Figure 1a). At 14 dpi a lower presence of mucins was observed in the infected glands (Figure 1b). At 21 dpi and at 60 dpe mucins re-emerged in the SMCs and MNCs to similar levels as in control animals. AB-PAS pH 2.5 stains neutral mucins in magenta, acidic mucins in blue and a mixture of the two in purple. In control animals (Figure 1e), the SMCs were found to produce a mixture of neutral and acidic mucins on the top of the fundic folds and in the gastric pits. Deeper in the gland, MNCs produced only acidic mucins. During infection, at 14 dpi, loss of staining was observed around the infected glands, while in the rest of the mucosa both the SMCs and MNCs produced a mixture of neutral and acidic mucins (Figure 1f). Similar results were obtained for the samples collected 21 dpi and 60 dpe (Figure 1g-h). Finally HID-AB staining for acidic mucins was performed, coloring the sialylated in blue and the sulfated in brown. In uninfected animals, sialylated mucins were identified in the superficial layer of the mucosa (SMCs) and a mixture of sulfated and sialylated in the gastric pits, while only sulfated mucins were observed in the neck region (MNCs) (Figure 1i). At 14 dpi (Figure 1l), less staining around the infected gland was observed. At 14 (Figure 1l), 21 dpi (Figure 1m) and at 60 dpe (Figure 1n) MNCs appear to produce not only sulfated mucins, as in control animals, but also sialylated ones.


Infection with the gastrointestinal nematode Ostertagia ostertagi in cattle affects mucus biosynthesis in the abomasum.

Rinaldi M, Dreesen L, Hoorens PR, Li RW, Claerebout E, Goddeeris B, Vercruysse J, Van Den Broek W, Geldhof P - Vet. Res. (2011)

Histochemical staining of Carnoy's fixed, paraffin-embedded abomasum sections of Holstein cows after Ostertagia ostertagi infection. PAS (A-D) stained mucins in pink; AB-PAS pH 2.5 (E-H) stained neutral mucins in magenta and acidic mucins in blue; HID-AB (I-N) stained sialylated mucins in blue and sulphated mucins in brown. (A, E, I) negative control, (B, F, L) infected for 14 days, (C, G, M) infected for 21 days, (D, H, N) exposed for 60 days. Original magnification 10×.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3102617&req=5

Figure 1: Histochemical staining of Carnoy's fixed, paraffin-embedded abomasum sections of Holstein cows after Ostertagia ostertagi infection. PAS (A-D) stained mucins in pink; AB-PAS pH 2.5 (E-H) stained neutral mucins in magenta and acidic mucins in blue; HID-AB (I-N) stained sialylated mucins in blue and sulphated mucins in brown. (A, E, I) negative control, (B, F, L) infected for 14 days, (C, G, M) infected for 21 days, (D, H, N) exposed for 60 days. Original magnification 10×.
Mentions: Histochemistry was performed to detect mucins in the mucosa of the abomasum during an infection with O. ostertagi (Figure 1). PAS, which stains all glycoproteins including mucins, was observed in surface mucus cells (SMCs) and mucus neck cells (MNCs) of uninfected animals (Figure 1a). At 14 dpi a lower presence of mucins was observed in the infected glands (Figure 1b). At 21 dpi and at 60 dpe mucins re-emerged in the SMCs and MNCs to similar levels as in control animals. AB-PAS pH 2.5 stains neutral mucins in magenta, acidic mucins in blue and a mixture of the two in purple. In control animals (Figure 1e), the SMCs were found to produce a mixture of neutral and acidic mucins on the top of the fundic folds and in the gastric pits. Deeper in the gland, MNCs produced only acidic mucins. During infection, at 14 dpi, loss of staining was observed around the infected glands, while in the rest of the mucosa both the SMCs and MNCs produced a mixture of neutral and acidic mucins (Figure 1f). Similar results were obtained for the samples collected 21 dpi and 60 dpe (Figure 1g-h). Finally HID-AB staining for acidic mucins was performed, coloring the sialylated in blue and the sulfated in brown. In uninfected animals, sialylated mucins were identified in the superficial layer of the mucosa (SMCs) and a mixture of sulfated and sialylated in the gastric pits, while only sulfated mucins were observed in the neck region (MNCs) (Figure 1i). At 14 dpi (Figure 1l), less staining around the infected gland was observed. At 14 (Figure 1l), 21 dpi (Figure 1m) and at 60 dpe (Figure 1n) MNCs appear to produce not only sulfated mucins, as in control animals, but also sialylated ones.

Bottom Line: Several genes involved in mucin core structure synthesis, branching and oligomerization, such as GCNT3, GCNT4, A4GNT and protein disulphide isomerases were found to be upregulated.Finally, transcription levels of 2 trefoil factors, TFF1 and TFF3, which are co-expressed with mucins in the GI tract, were also found to be significantly upregulated in infected animals.Although the alterations in mucus biosynthesis started early during infection, the biggest effects were found when adult worms were present on the surface of the abomasal mucosa and are likely caused by the alterations in mucosal cell populations, characterized by hyperplasia of mucus secreting cells.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium. peter.geldhof@UGent.be.

ABSTRACT
The mucus layer in the gastrointestinal (GI) tract is considered to be the first line of defense to the external environment. Alteration in mucus components has been reported to occur during intestinal nematode infection in ruminants, but the role of mucus in response to abomasal parasites remains largely unclear. The aim of the current study was to analyze the effects of an Ostertagia ostertagi infection on the abomasal mucus biosynthesis in cattle. Increased gene expression of MUC1, MUC6 and MUC20 was observed, while MUC5AC did not change during infection. Qualitative changes of mucins, related to sugar composition, were also observed. AB-PAS and HID-AB stainings highlighted a decrease in neutral and an increase in acidic mucins, throughout the infection. Several genes involved in mucin core structure synthesis, branching and oligomerization, such as GCNT3, GCNT4, A4GNT and protein disulphide isomerases were found to be upregulated. Increase in mucin fucosylation was observed using the lectin UEA-I and through the evaluation of fucosyltransferases gene expression levels. Finally, transcription levels of 2 trefoil factors, TFF1 and TFF3, which are co-expressed with mucins in the GI tract, were also found to be significantly upregulated in infected animals. Although the alterations in mucus biosynthesis started early during infection, the biggest effects were found when adult worms were present on the surface of the abomasal mucosa and are likely caused by the alterations in mucosal cell populations, characterized by hyperplasia of mucus secreting cells.

Show MeSH
Related in: MedlinePlus