Immunomodulatory effects of dietary protein during <i>Nippostrongylus brasiliensis</i> re‐infection in lactating rats

Jones, Leigh Ann; Houdijk, J.G.M.; Knox, Dave P.; Kyriazakis, Ι.

doi:10.1111/j.1365-3024.2009.01121.x

Cited by 19 publications

(28 citation statements)

References 44 publications

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“…Results presented here indicate for the first time that nutrient supplementation can affect immune responses during the lung phase of Nb infection. Hence, previously observed benefits of dietary protein supplementation (1,2) may already be generated during the lung phase of the infection. …”

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Effect of dietary protein supplementation on gene expression in the lung of lactating rats infected with Nippostrongylus brasiliensis

et al. 2016

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Previous studies have shown that the breakdown of immunity to Nippostrongylus brasiliensis (Nb), a rat nematode used as a model for gastrointestinal parasitism, is sensitive to dietary protein supply, as measured at the small intestine, the parasite niche (1,2) . Nb however goes through systemic migration, entering host's skin and migrating to lung parenchyma through blood vessels before reaching the intestine. Here we investigated for the first time the effect of dietary protein supply on host's lung in the Nb re-infected rat model.Nulliparous female Sprague-Dawley rats were given primary infection of 1600 Nb 3 rd stage infective larvae (L3) subcutaneously 14 days prior to mating. Ten days post mating confirmation, rats were offered ad libitum access to either a High Protein (H) or a Low Protein (L) diet until sampling point. Half of these animals were administered with a secondary 1600 L3 on day 2 post parturition (pp) defined as Nb + Nb group (L n = 9, H n = 7), whereas the other half were injected with PBS, defined as Nb + PBS group (L and H n = 6). Animals that did not receive primary and secondary infections were placed as a naïve control (L and H n = 3). Expression of genes related to lung inflammation, particularly alternatively activated macrophages (AAMs) including, arginase 1 (Arg1), resistin-like molecules α (Retnla), and matrix metalloproteinase MMP-12 (Mmp12), and a marker for classically activated macrophages (CAMs), inducible nitric oxide synthase (Nos2), was measured in the lung on day 5 pp. Data were analysed by 2 (diets) × 3 (infection status) ANOVA.Retnla expression was significantly higher in H compared to L animals following secondary infection (P < 0·001), and Mmp12 expression tended to be higher in H animals (P = 0·059). Dietary protein did not have significant effect on Arg1 and Nos2 expression. Expression of Retnla and Mmp12 were significantly up-regulated following secondary infection (P < 0·001). Arg1 tended to be higher (P = 0·076) following secondary infection whereas Nos2 expression was significantly down regulated (P < 0·001) after secondary infection.Despite the fact that the intestine is a critical site for immune response development, studies in mice have shown that the lung phase plays a crucial role in generating immunity against Nb re-infection (3,4) . Results presented here indicate for the first time that nutrient supplementation can affect immune responses during the lung phase of Nb infection. Hence, previously observed benefits of dietary protein supplementation (1,2) may already be generated during the lung phase of the infection.

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Effect of dietary protein supplementation on gene expression in the lung of lactating rats infected with Nippostrongylus brasiliensis

et al. 2016

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“…It has indeed been shown that Nippostrongylus brasiliensis re-infected lactating rats fed low-crude protein (N · 6.25; CP) diets showed an augmented extent of PPRI compared with their high-protein-fed counterparts (2) . However, effects of CP intake were confounded with metabolizable energy (ME) intake as a result of increased food intake on the high-protein diets.…”

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Resistance to parasites in lactating rats is sensitive to protein but not energy supply

Sakkas¹,

Jones²,

Houdijk³

et al. 2009

Proc. Nutr. Soc.

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Periparturient relaxation of immunity (PPRI) to parasites in mammals results in increased worm burdens and worm egg excretion and may have a nutritional basis (1) . It has indeed been shown that Nippostrongylus brasiliensis re-infected lactating rats fed low-crude protein (N · 6.25; CP) diets showed an augmented extent of PPRI compared with their high-protein-fed counterparts (2) . However, effects of CP intake were confounded with metabolizable energy (ME) intake as a result of increased food intake on the high-protein diets. Here, effects of CP and ME supply on PPRI were independently assessed.Second-parity rats were infected with 1600 N. brasiliensis larvae before mating (primary infection). On parturition dams were allocated to one of six feeding treatments (1-6) consisting of two levels of ME supply at one of three levels of CP supply; feeding treatments were balanced for parturition body weight (PBW; n 14). Feeding treatments 1, 2 and 3 were calculated to supply 1.05 MJ ME/kg PBW per d, whereas treatments 4, 5 and 6 were calculated to supply 1.40 MJ ME/kg PBW per d. In addition, CP supply was calculated to incrementally increase from scarce to more than adequate at each level of ME intake: 6.6, 13.3 and 19.9 g/kg PBW per d for feeding treatments 1, 2 and 3 respectively; 13.3, 19.9 and 26.5 g/kg PBW per d for treatments 4, 5 and 6 respectively. Rats were re-infected with 1600 N. brasiliensis larvae on day 2 of lactation (secondary infection), when litter size was standardized at ten pups. Dams and litters were weighed daily until either on day 8 or day 11 of lactation when worm burdens (number and gender) were assessed as a proxy for PPRI.

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Nutritional regulation of resistance to Nippostrongylus brasiliensis re-infection in lactating rats

et al. 2015

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Previous studies in small ruminants and rodents have shown that breakdown of immunity to gastrointestinal nematode (GIN) infection occurs during parturition (1) , and this breakdown is believed to have a nutritional basis (2,3) . Local and systemic immune responses are essential for the initiation of a Type 2 (Th2) immune response, which results in parasite expulsion (4) . Here we investigated the impact of dietary protein supply on systemic responses in a Nippostrongylus brasiliensis re-infection lactating rat model.Multiparous female Sprague-Dawley rats were given a primary infection of 1600 N. brasiliensis 3 rd stage infective larvae (L3) subcutaneously 14 days prior to mating. Ten days post mating confirmation, rats were offered either a High Protein (H) or a Low Protein (L) diet through the latter half of gestation and during lactation. Half of these animals were administered with a secondary 1600 L3 on day 2 post parturition (pp), whereas the other half were sham-infected controls. Expression of genes related to Th1, such as interferon (IFN)-γ, Th2, such as interleukin (IL)-13 and arginase 1, and anti-inflammatory agents, such as peroxisome proliferator activated receptor (PPAR)-γ and 12/15 lipoxygenase, was measured in the spleen on day 5 pp.There was a significant feeding treatment by time interaction on dam weight ( Fig. 1; P < 0·05) over the latter half of the gestation period, and pup weight during lactation, with H diet resulting in heavier dams and pups. Gene expression in the spleen, including IL-13 (Fig. 2), arginase 1 (Fig. 2), 12/15 lipoxygenase, PPAR-γ and IFN-γ, was significantly up-regulated in H compared to L animals (P < 0·05). Infection status did not have significant effect on dam or pup weight and gene expression.The spleen has shown to be an important source of Th2 cells in GIN infection (4) . Up-regulation of Th2 genes in both challenged and non-infected H groups suggests that high protein diet intake during gestation and lactation can improve both maternal performance and immune responses. It is still largely unknown how these effects are mediated, and further understanding of these mechanisms is important for developing practical and sustainable nutritional parasite control strategies in mammals.

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Immunomodulatory effects of dietary protein during Nippostrongylus brasiliensis re‐infection in lactating rats

Cited by 19 publications

References 44 publications

Effect of dietary protein supplementation on gene expression in the lung of lactating rats infected with Nippostrongylus brasiliensis

Effect of dietary protein supplementation on gene expression in the lung of lactating rats infected with Nippostrongylus brasiliensis

Resistance to parasites in lactating rats is sensitive to protein but not energy supply

Nutritional regulation of resistance to Nippostrongylus brasiliensis re-infection in lactating rats

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