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Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity.

Li Z, Zhang S, Liu Q - PLoS ONE (2008)

Bottom Line: Vitellogenin (Vg), a major reproductive protein, has been associated with infection-resistant response in fish.This study shows that fish Vg plays an integrative function in regulating immunity via its pleiotropic effects on both recognizing pathogen-associated molecular patterns and promoting macrophage phagocytosis.It also supports the notion that factors normally involved in control of female reproduction are associated with immunity in organisms that rely on Vg for oocyte development.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology, Ocean University of China, Qingdao, People's Republic of China.

ABSTRACT

Background: Vitellogenin (Vg), a major reproductive protein, has been associated with infection-resistant response in fish. However, the underlying mechanisms by which Vg is involved in anti-infectious response are not understood.

Methodology/results: By both protein-microbe interaction analysis and enzyme-linked immunosorbent assay as well as phagocytosis test, we demonstrate for the first time that fish Vg acts as a pattern recognition molecule with multiple specificities that can recognize bacteria as well as fungus rather than self components from fish, and functions as an opsonin that can enhance macrophage phagocytosis.

Conclusions: This study shows that fish Vg plays an integrative function in regulating immunity via its pleiotropic effects on both recognizing pathogen-associated molecular patterns and promoting macrophage phagocytosis. It also supports the notion that factors normally involved in control of female reproduction are associated with immunity in organisms that rely on Vg for oocyte development.

Show MeSH
Phagocytic ability (PA) and phagocytic index (PI) of macrophages engulfing E. coli, S. aureus and P. pastoris.Both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Phagocytosis was observed at 60 min after mixing macrophages with microbes. The microbes pre-incubated with Vg were readily phagocytosed by the macrophages, while those precubated with BSA or PBS alone were not. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were significantly higher than those of the cells phagocytosing BSA-treated and untreated microbes (p<0.05). There was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. Data are expressed as mean values±SEM from three experiments. The bars represent the standard error of the mean, and asterisks denote statistically significant differences (p<0.05). (A) PA of macrophages engulfing E. coli, S. aureus and P. pastoris. (B) PI of macrophages engulfing E. coli, S. aureus and P. pastoris.
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pone-0001940-g005: Phagocytic ability (PA) and phagocytic index (PI) of macrophages engulfing E. coli, S. aureus and P. pastoris.Both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Phagocytosis was observed at 60 min after mixing macrophages with microbes. The microbes pre-incubated with Vg were readily phagocytosed by the macrophages, while those precubated with BSA or PBS alone were not. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were significantly higher than those of the cells phagocytosing BSA-treated and untreated microbes (p<0.05). There was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. Data are expressed as mean values±SEM from three experiments. The bars represent the standard error of the mean, and asterisks denote statistically significant differences (p<0.05). (A) PA of macrophages engulfing E. coli, S. aureus and P. pastoris. (B) PI of macrophages engulfing E. coli, S. aureus and P. pastoris.

Mentions: The macrophage population isolated from the head kidney (front part of fish kidney) of H. otakii had a viability of about 98%. To examine if Vg promotes macrophage phagocytosis, both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Pilot experiments showed that both phagocytic ability (PA) and phagocytic index (PI) reached maximum values at 60 min after incubation of macrophages with microbes, and the engulfed microbes became digested to pieces at 105 min (Fig. 4). Therefore, phagocytosis was observed at 60 min after mixing macrophages with microbes in subsequent experiments. Compared with the microbes pre-incubated with BSA and PBS alone, those pre-incubated with Vg were readily phagocytosed by the macrophages. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were 56.0±3.5%, 49.0±2.0% and 42.0±2.4%, and 2.920±0.072, 2.333±0.113 and 1.677±0.118, respectively, while the PA and PI values of the cells engulfing BSA-treated and untreated E. coli, S. aureus and P. pastoris were 36.0±1.7%, 35.0±2.0% and 32.0±1.8%, and 36.3±1.8%, 36.9±1.2% and 34.5±1.3%, and 0.831±0.065, 1.740±0.179 and 1.060±0.049, and 0.836±0.049, 1.719±0.046 and 0.991±0.015, individually (Fig. 5). Apparently, the percent of macrophages phagocytosing Vg-treated microbes was significantly higher than that of cells phagocytosing BSA-treated and untreated microbes (p<0.05). Furthermore, the number of Vg-treated microbes engulfed by each macrophage was also significantly higher than that of BSA-treated and untreated microbes engulfed by each macrophage (p<0.05). In contrast, there was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. These denoted that Vg is able to promote the macrophage phagocytosis.


Vitellogenin functions as a multivalent pattern recognition receptor with an opsonic activity.

Li Z, Zhang S, Liu Q - PLoS ONE (2008)

Phagocytic ability (PA) and phagocytic index (PI) of macrophages engulfing E. coli, S. aureus and P. pastoris.Both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Phagocytosis was observed at 60 min after mixing macrophages with microbes. The microbes pre-incubated with Vg were readily phagocytosed by the macrophages, while those precubated with BSA or PBS alone were not. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were significantly higher than those of the cells phagocytosing BSA-treated and untreated microbes (p<0.05). There was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. Data are expressed as mean values±SEM from three experiments. The bars represent the standard error of the mean, and asterisks denote statistically significant differences (p<0.05). (A) PA of macrophages engulfing E. coli, S. aureus and P. pastoris. (B) PI of macrophages engulfing E. coli, S. aureus and P. pastoris.
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pone-0001940-g005: Phagocytic ability (PA) and phagocytic index (PI) of macrophages engulfing E. coli, S. aureus and P. pastoris.Both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Phagocytosis was observed at 60 min after mixing macrophages with microbes. The microbes pre-incubated with Vg were readily phagocytosed by the macrophages, while those precubated with BSA or PBS alone were not. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were significantly higher than those of the cells phagocytosing BSA-treated and untreated microbes (p<0.05). There was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. Data are expressed as mean values±SEM from three experiments. The bars represent the standard error of the mean, and asterisks denote statistically significant differences (p<0.05). (A) PA of macrophages engulfing E. coli, S. aureus and P. pastoris. (B) PI of macrophages engulfing E. coli, S. aureus and P. pastoris.
Mentions: The macrophage population isolated from the head kidney (front part of fish kidney) of H. otakii had a viability of about 98%. To examine if Vg promotes macrophage phagocytosis, both Vg in PBS and BSA in PBS as well as PBS alone were pre-incubated with the FITC-labeled microbes, E. coli, S. aureus and P. pastoris, and then incubated with the macrophages freshly isolated. Pilot experiments showed that both phagocytic ability (PA) and phagocytic index (PI) reached maximum values at 60 min after incubation of macrophages with microbes, and the engulfed microbes became digested to pieces at 105 min (Fig. 4). Therefore, phagocytosis was observed at 60 min after mixing macrophages with microbes in subsequent experiments. Compared with the microbes pre-incubated with BSA and PBS alone, those pre-incubated with Vg were readily phagocytosed by the macrophages. The PA and PI values of the macrophages phagocytosing Vg-treated E. coli, S. aureus and P. pastoris were 56.0±3.5%, 49.0±2.0% and 42.0±2.4%, and 2.920±0.072, 2.333±0.113 and 1.677±0.118, respectively, while the PA and PI values of the cells engulfing BSA-treated and untreated E. coli, S. aureus and P. pastoris were 36.0±1.7%, 35.0±2.0% and 32.0±1.8%, and 36.3±1.8%, 36.9±1.2% and 34.5±1.3%, and 0.831±0.065, 1.740±0.179 and 1.060±0.049, and 0.836±0.049, 1.719±0.046 and 0.991±0.015, individually (Fig. 5). Apparently, the percent of macrophages phagocytosing Vg-treated microbes was significantly higher than that of cells phagocytosing BSA-treated and untreated microbes (p<0.05). Furthermore, the number of Vg-treated microbes engulfed by each macrophage was also significantly higher than that of BSA-treated and untreated microbes engulfed by each macrophage (p<0.05). In contrast, there was no significant difference in the PA and PI values of the cells engulfing BSA-treated and untreated microbes. These denoted that Vg is able to promote the macrophage phagocytosis.

Bottom Line: Vitellogenin (Vg), a major reproductive protein, has been associated with infection-resistant response in fish.This study shows that fish Vg plays an integrative function in regulating immunity via its pleiotropic effects on both recognizing pathogen-associated molecular patterns and promoting macrophage phagocytosis.It also supports the notion that factors normally involved in control of female reproduction are associated with immunity in organisms that rely on Vg for oocyte development.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology, Ocean University of China, Qingdao, People's Republic of China.

ABSTRACT

Background: Vitellogenin (Vg), a major reproductive protein, has been associated with infection-resistant response in fish. However, the underlying mechanisms by which Vg is involved in anti-infectious response are not understood.

Methodology/results: By both protein-microbe interaction analysis and enzyme-linked immunosorbent assay as well as phagocytosis test, we demonstrate for the first time that fish Vg acts as a pattern recognition molecule with multiple specificities that can recognize bacteria as well as fungus rather than self components from fish, and functions as an opsonin that can enhance macrophage phagocytosis.

Conclusions: This study shows that fish Vg plays an integrative function in regulating immunity via its pleiotropic effects on both recognizing pathogen-associated molecular patterns and promoting macrophage phagocytosis. It also supports the notion that factors normally involved in control of female reproduction are associated with immunity in organisms that rely on Vg for oocyte development.

Show MeSH