Effects of lotus plumule supplementation before and following systemic administration of lipopolysaccharide on the splenocyte responses of BALB/c mice

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Abstract

To determine whether lotus plumule supplementation alleviates acute systemic inflammation in vivo, the BALB/c mice were continuously supplemented with lotus plumule for 3 weeks, following administration with an intraperitoneal (i.p.) injection of lipopolysaccharide (LPS) at a concentration of 10 mg/kg body weight (BW) to induce acute systemic inflammation. At 24 h after injection of LPS, the mice were sacrificed and the visceral organ weight and splenocyte responses were measured. The results showed that lotus plumule supplementation did not significantly affect body weights and IL-6 secretion of splenocyte cultures from BALB/c mice. LPS challenge significantly increased the relative organ weights of the lungs, liver, and spleen, however low dose supplementation (40 mg/kg BW/day) with lotus plumule significantly decreased the relative organ weights of the inflammatory liver, spleen and kidney. Low dose supplementation with lotus plumule significantly increased IL-10 production of splenocyte cultures, however high dose supplementation (800 mg/kg BW/day) significantly decreased IL-10 production. These results suggest that low dose and 3-week supplementation of lotus plumule might alleviate acute systemic inflammation in vivo via decreasing the visceral organ inflammation and increasing the production of anti-inflammatory cytokine IL-10 from splenocytes. These results are valuable for developing future nutraceuticals and anti-inflammatory agents from traditional medicinal foods.

Introduction

An uncontrolled inflammatory response is believed to be the cause of systemic inflammatory response syndrome (SIRS), sepsis and other clinical conditions related to sepsis. Severe sepsis may result in shock which is a complication of sepsis with a high mortality rate of 40–60%. Sepsis is a complex program influenced by multiple factors, including environmental, physiological, genetic background, and immunological conditions etc. (De Maio et al., 1998, Stewart et al., 2002). Three most influential mediators appear to be tumor necrosis factor (TNF)-α, interleukin (IL)-1 and IL-6 during SIRS/sepsis (Davies and Hagen, 1997). TNF-α, and IL-1 are usually regarded as pro-inflammatory cytokines (Kim et al., 2004b) and IL-6 is suggested to play a critical role in the manifestation of fever (Roth et al., 2004). Besides, nitric oxide (NO) and prostaglandin E2 (PGE2) produced from lipopolysaccharide (LPS)-induced inflammatory cells, especially macrophages or chondrocytes, are also regarded as pro-(Kim et al., 2005) or secondary inflammatory mediators (Davies and Hagen, 1997) during inflammation. However, IL-10 is a cytokine that exhibits potent anti-inflammatory activities via inhibiting the synthesis of pro-inflammatory cytokines, the release of reactive oxygen and nitrogen intermediates, and the antigen-presenting capacity of mononuclear phagocytes or dendritic cells (Emmanuilidis et al., 2001). Other cytokines such as IL-2, IL-4, IL-8, interferon (IFN)-γ, and granulocyte/macrophage colony stimulating factors (GM-CSF) may participate in the systemic inflammation with synergistic or antagonistic actions.

Inflammatory responses in mice have found to be affected by sex, age, and other nongenetic components such as diet (De Maio et al., 2005). However, anti-inflammatory treatment strategies, such as IL-10 (Emmanuilidis et al., 2001), ascorbic acid (Victor et al., 2000), retinoids (Kim et al., 2004a), α-tocopherol (Berg et al., 2004), traditional herbal medicine (Kim et al., 2000), might provide host defenses in different situations of sepsis or severe inflammation. Ancient Chinese herbal medicine might provide a modern hope for the treatment of sepsis or acute systemic inflammation. Almost all parts of the lotus plant are used as folk medicine and also eaten as vegetable. Lotus seeds, as a vegetable, are currently sold in the Indian market in the name of kamal gatta, (Anonymous, 1992). Lotus plumule, a medicinal food and traditional Chinese medicine, is now available with commercial forms of powder, cut, and concentrates in market. Lotus plumule is used as tea, or powder supplement for the purpose of health. The use of lotus plumule as a folk medicine in Chinese can be backdated to the description by a well-known pharmacopoeia, Pen-Tsao-Kang-Mu of Lee Hsih-Jen in the Ming Dynasty. Thus far, the use of lotus plumule spreads in Asia. Lotus plumule was traditionally introduced into Chinese medicine as an anti-inflammatory agent in Taiwan. It has been reported that lotus seed is effective in antioxidant properties and protecting DNA damage in human lymphocytes (Yen et al., 2005a). However, the effect of lotus plumule on acute systemic inflammation has not been fully explored yet. As lotus plumule is a daily supplement taken by many people in Taiwan, we investigated the prophylactic effects of lotus plumule on acute systemic inflammation (Lin et al., 2006).

Recently, animal models with injection of E. coli LPS or polymicrobial sepsis induced by cecal ligation and puncture (CLP) were introduced to evaluate the effects of medicine, foods, or nutrition on systemic inflammation (Oberbeck et al., 2003, Saito et al., 2003, Yeh et al., 2005). LPS can interact with LPS binding protein (LBP) and bactericidal/permeability increasing protein (BPI). The LBP interacts with the LPS receptor CD14 inducing cytokine expression (Davies and Hagen, 1997). Thus, intraperitoneal injection of endotoxin LPS might induce systemic inflammation.

To determine whether lotus plumule has prophylactic effects on acute systemic inflammation in vivo, an inbred strain murine model was supplemented with lotus plumule powder for 3 weeks before systemic administration of LPS, following peritoneal injection of endotoxin LPS. After LPS challenge for 24 h, the mice were sacrificed and the splenocyte responses were measured.

Section snippets

Sample preparation

The most widely cultivated lotus species is Nelumbo nicifera Geartn in Taiwan. Thus, this lotus species was chosen to conduct in this study. Briefly, fresh lotus seeds from a variety of Nelumbo nucifera Geartn. were provided by a farmer in Tainan, Taiwan. The lotus plumule was carefully collected and then air dried at 40 °C overnight. The air-dried lotus plumule was milled into powder, then placed into plastic bottles and stored at −20 °C until use.

Experimental animals and dietary groups

The female BALB/c mice (6 weeks old) were

Effects of lotus plumule supplementation on body and visceral organ weights of LPS-challenged mice

In this study, the female BALB/c mice were fed with lotus plumule powder for 3 weeks and then administrated with LPS i.p. to induce systemic inflammation. The results showed that lotus plumule supplementation did not significantly affect the body weight among groups during the regular feeding experimental period. The body weights of SC, DC, L, and H groups changed from 24.4 ± 2.6 to 24.7 ± 1.4 g, from 25.0 ± 4.2 to 25.9 ± 3.2 g, from 24.3 ± 2.4 to 25.5 ± 1.9 g, and from 24.4 ± 2.1 to 24.0 ± 2.8 g, respectively.

Discussion

The aim of this study was to determine the effects of lotus plumule supplementation on systemic inflammation in vivo using a LPS-challenged mouse model. We attempted to establish a mild systemic inflammation model induced by LPS to evaluate the anti-inflammatory effects of health foods. Victor et al. (2000) have reported that female BALB/c mice administrated i.p. with LPS at a concentration of 100 mg/kg BW resulted in lethal endotoxic shock. However, challenge with LPS at the dosage of 15 mg/kg

Conclusion

This study showed that low dose and 3-week supplementation with lotus plumule before acute systemic inflammation significantly decreased the relative visceral organ weights of the enlarged liver, spleen and kidney which resulted from systemic administration of LPS. Low dose supplementation with lotus plumule in vivo significantly increased IL-10 production and cell proliferation in splenocyte cultures from LPS-challenged mice. These results suggest that low dose supplementation of lotus plumule

Acknowledgement

This study was supported by a research grant NSC93-2313-B-005-033 from the National Science Council, Taipei, Taiwan, Republic of China (ROC).

References (27)

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