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Berberine-Induced Amelioration of the Pathological Changes in Nutrients Homeostasis During Murine Intestinal Eimeria papillata Infection.

Byline: Saleh Al-Quraishy, Nour E. Sherif, Mahmoud S. Metwaly and Mohamed A. Dkhil

Abstract.- The current work aimed to study the ameliorative effect of berberine on the induced pathological changes in nutrients homeostasis in mice infected with Eimeria papillata. Mice were randomly divided into three groups. The first group represents the control non-infected animals. Second and third groups were orally infected with1.5A-103 sporulated E. papillata oCysts. The 3rd group was treated with a daily dose (10 mg/kg) of berberine chloridesolution for five successive days. All animals were sacrificed on day 5 p.i.. E. papillata infection induced a state of disturbance in nutrient homeostasis. Blood glucose levels and total proteins were elevated with concurrent decrease in level of carbohydrates and soluble proteins in jejunum of mice. Also, infection induced a hyperlipidemic status as shown from the increase in triglycerides, total lipids, total cholesterol, high density lipoprotein cholesterol (LDL) with the mutual decrease in high density lipoprotein cholesterol (HDL) and phospholipids. Also, E. papillata caused marked disturbance in blood metal ion concentrations. Both ferrous and selenium ion levels were decreased, while sodium and potassium ion concentrations were increased. Berberine treatment of infected mice with E. papillata showed a great enhancement in nutrient homeostatic status and also reduced blood glucose level and restored jejunal carbohydrate content. In addition, berberine exerted hypolipidemic effect on the increased fractions of carbohydrates and lipids. Finally, berberine showed a marked enhancement in the levels of altered blood metal ions by the infection. Palm pollen grains or their extracts could be used within food mixtures or water to correct the induced metabolic disturbance and growth depression assCiated with the intestinal cCcidial infections.

Key words: Berberine, cCcidiosis, impaired nutrients, Eimeria papillata, mice.

INTRODUCTION

Eimeriosis is a cosmopolitan serious disease infecting nearly all mammal species. Its causal agent (Sporozoites) reproduce via fast and invasive multiplication within intestinal tract causing tissue damage and induce severe lCal and systemic inflammatory response (Al-Quraishi et al.,2012; Dkhil et al., 2012) leading to diminished feed intake and nutrient absorption, reduced body-weight gain, dehydration, blood loss, and increased susceptibility to other diseases in different animal communities. Thus, it causes huge economic loss in the field of animal farming, milk and meat production (Bhat et al., 1996; Dkhil and Al- Quraishi, 2012). Eimeria papillata parasitize mice and provides a convenient model for studyinganimal cCcidiosis as its intracellular development within mice jejunum is rapid resulting in fecal oCyst output on day 3 p.i. (Stafford and Sundermann, 1991; Schito and Barta, 1997).The necessity appears to use traditional medicines of natural plant origin to avoid the problems with drug resistance and the adverse side effects of synthetic drug therapy. Currently, new trends have been developed to identify various dietary supplements of natural origin into feeding programs to control Eimeria infections (Abbas et al., 2011; Metwaly et al., 2012; Dkhil et al., 2013).Berberine is an isoquinoline alkaloid, presentin roots and stem-bark of clinically important medicinal plants (Wongbutdee, 2008; Vuddanda et al., 2010; Amer et al., 2013). Berberine based formulations, are widely used in traditional systems of medicine including, Ayurveda and Traditional Chinese Medicine. Berberine has demonstrated wide range of pharmacological activities. It has significant antimicrobial activity against a variety of organisms including bacteria, virus, fungi, protozoa,helminths and Chlamydia. Other physiological activities of berberine being antihypertensive, anti- inflammatory, antioxidant, antidepressant, anticancer, anti-diarrhoeal, cholagogue and hepatoprotective. In addition, berberine is not considered to be toxic at doses used in clinical situations, nor has been shown to be cytotoxic or mutagenic (Wongbutdee, 2008; Vuddanda et al.,2010).The current study was aimed to investigatethe impact of berberine administration to mice infected with E. papillata upon lipid, protein, carbohydrate and metal ion status.

MATERIALS AND METHODS

Preparation of E. papillata oCystsA self-healing strain of E. papillata was kindly provided by Prof. Mehlhorn of Heinrich Heine University, Duesseldorf, Germany. Several passage prCesses of E. papillata were performed in laboratory mice (Mus musculus), followed by oCyst collection from faeces and sporulation prCess in potassium dichromate solution (2.5%). After that, the sporulated oCysts were washed several times with sterile saline and then surface-sterilized with sodium hypChlorite, and washed at least four times with sterile saline before oral inCulation as described by Schito and Barta (1997). These oCysts were used to inCulate mice by oral gavaging each mouse with 1.5A-103 sporulated oCysts of E. papillata suspended in 100 l sterile saline.

Berberine chloride treatmentBerberine chloride was purchased from Sigma Company (St Louis, MO, USA). Each mouse was orally inCulated with 10 mg/kg body weight berberine chloride. The used dose is in agreement with previous studies on other intestinal protozoan infections and toxicity measurements (Jahnke et al.,2006).

Animals and experimental designEighteen male Swiss albino mice (9-11weeks) randomly divided into three groups (Six mice/each group). The first group received saline and served as a non-infected control group. Second and third groups were orally infected with 1.5A-103 sporulated E. papillata oCysts. The 3rd group was treated with a daily dose of berberine chloride for five successive days. The experiments were approved by state authorities and followed Saudi Arabian rules for animal protection. Weight change of mice was recorded during the experimental time and at the end of the experiment.

Sample collectionAnimals were cervically dislCated on day 5 p.i. and the blood was collected from heart into heparinized tubes. Plasma was separated and kept at-20C until use. Parts of jejunum were weighed and homogenized immediately in ice-cold phosphate buffered saline then centrifuged at 2000 g.A-15 min at 4C to give a final yield of (10% w/v) jejunal homogenate that were kept at -20 C until use.

Blood biChemical analysisBlood plasma was analyzed using commercial kits (Biomerieux, Marcy lEtoil, France) for glucose (Trinder, 1969a) and total proteins (Gornall et al., 1949). While, jejunum homogenate was used for the determination of total carbohydrate content using phenol-sulfuric acid method (Dubois et al., 1979) and for measuring soluble protein content (Lowry et al., 1951). In addition, plasma lipid fractions were assayed colorimetrically using commercially available kits (Biodiagnostic company, Giza, Egypt) for total lipids (Knight et al., 1972), total cholesterol (Trinder, 1969b), high-density lipoprotein (HDLc) cholesterol (Trinder, 1969b), phospholipids (Zilversmit and Davies, 1950), and triglycerides (T.Gs) (Fossati and Principe, 1982). Low-density lipoprotein (LDL) cholesterol and very low density lipoprotein (VLDL) cholesterol were calculated according to Van Horn et al. (1988).Plasma samples from all groups weredigested with concentrated nitric acid and hydrogen peroxide as described by Bukhari et al. (2005). Levels of iron (Fe), potassium (K), sodium (Na), and selenium (Se) were determined using the atomic emission spectrometer with inductivity coupled plasma iCAP-6500 Duo (Thermo scientific, United Kingdom).HistChemical studies of jejunumSmall pieces of the jejunum were quickly removed, then fixed in 10 % neutral buffered formalin. Following fixation, specimens were dehydrated, embedded in wax, and then sectioned to5m thickness. Then sections were stained with periodic acid-Schiffs method for total carbohydrates demonstration (Hotchkiss, 1948), and with mercuric bromophenol blue method to demonstrate total proteins (Maize et al., 1953).

Statistical analysisOne-way ANOVA was carried out, and the statistical comparisons among the groups were performed with Duncans test using a statistical package program (SPSS version 17.0). All p values are twoTailed and P less than 0.05 was considered as significant for all statistical analysis in this study.

RESULTS

Experimental cCcidial infection in mice with E. papillata in both infected and infected treated groups was established as revealed oCyst discharging in faecal pellets beginning from day 3 p.i. and reached maximal level at day 5 p.i. (Un- published data).Examination of carbohydrate status revealedand increase in blood glucose level from 593.2 to684.2 mg/dl (Fig. 1). This increase was assCiated with depletion in the carbohydrate content within jejunum tissue from 77 to 68.3 mg/g (Figs. 2, 3). Oral administration of berberine chloride caused a significant decrease in blood glucose level in infected group to be 492.9 mg/dl (Fig. 1). Also, carbohydrate content in jejunum tissue was changed to be 123.8 mg/g in infected treated group (Figs. 2,3).Experimental infection of mice with E. papillata caused an increase in plasma total proteins and albumin from 4.80.25 and 1.870.21 to5.720.6 g/dl and 2.670.21 g/dl (Fig. 4),respectively. This was assCiated with depletion of jejunal soluble protein content from 152.518.4 to107.412.8 mg/g (Figs. 5, 6). Oral treatment of micewith berberine did not cause a significant change in plasma protein levels but it caused a significant increase in jejunal soluble proteins to be 166.4 mg/g in infected group (Figs. 4-6).cholesterol from 82.96.2 mg/dl to 754.7 and that of phospholipids from 7.20.3 to 4.70.23 mg/dl (Table I). In addition, both harmful fractions LDL cholesterol and VLDL cholesterol from 10.2 mg/dl and 12.8 mg/dl to 50.6 mg/dl and 15.6 mg/dl, respectively (Table I). Berberine showed an obvious diminishing the level of total lipids, total Cholesterol, triglycerides, LDL cholesterol and VLDL cholesterol nearby the control value of non- infected animals. Also, HDL cholesterol and phospholipids were restored more than the control value (Table I).

Table I.-###Berberine induced changes in plasma lipid

###fractions in mice infected with E. papillata on

###day 5 p.i.

Parameters###Non-infected###Infected

(mg/d)###- Berberine###- Berberine###+ Berberine

Total lipids###37110.3###479.110.5 a###339.88.3 a,b

Total###105.95.1###141.25.3 a###1205 a,b

cholesterol

Triglycerides###648###784.6 a###444 a,b

HDL-###82.97.5###754.8 a###1005.9 a,b

cholesterol

LDL-###10.20.75###50.63.75 a###11.20.65 b

cholesterol

VLDL-###12.80.8###15.60.65 a###8.80.45 a,b

cholesterol

Phospholipids###7.20.48###4.70.55 a###7.90.6 b

Table II.-###Berberine induced changes in plasma metal ion

###concentrations in mice infected with E.

###papillata on day 5 p.i.

###Non-infected###Infected###Infected

###(-Berberine)###(-Berberine)###(+Berberine)

Ferrous###39.91###30.70.9 a###35.11.1 a,b

(g/ml)

Potassium###166.56.5###219.88.8 a###142.95 a,b

(g/ml)

Sodium###975.350.5###1512.7107.5 a###1033.316.5 b

(g/ml)

The infection caused a marked disturbance in the metal ion concentration within blood. Ferrous and Selenium levels were markedly decreased by 23 and 30% respectively. In addition, both potassium and sodium ion concentration was significantly increased from 166.5 and 975.3 g/ml to 219.8 and1512.7 g/ml, respectively. Berberine couldsignificantly increase Fe and Se levels to be 35.1and 1.9 g/ml, respectively and decreased theincrease in Na and K ion levels to 1033.3 and 142.9g/ml, respectively (Table II).

DISCUSSION

The current work was designed to explore the effect of berberine treatment on infected mice with intestinal E. papillata infection upon the homeostatic status of lipids, proteins, carbohydrates and metal ions.E. papillata induced a hyperlipidemic status in infected mice as seen from the increased concentrations of plasma total lipids, total cholesterol, triglycerides, LDL cholesterol and VLDL cholesterol with concurrent decrease in HDL cholesterol and phospholipids. Upon treatment of infected mice with berberine solution, it was found that berberine has a strong hypolipidemic activity. It could significantly decrease total lipids, total cholesterol, riglyceride, LDL cholesterol and VLDL cholesterol, with mutual increase in HDL cholesterol and phospholipids.The increased lipid fractions in blood of mice infected with E. papillata parasite may be due to the disturbed energy homeostatic status by such infection which leads to stress-induced secretion of pancreatic glucagon and adrenal glucCortecoides that in turn activates both gluconeogenesis prCesses leading to breakdown of liver carbohydrate store (Feritas et al., 2008; Patra et al., 2009; Mondal et al., 2011), followed by increased rate of fat mobilization and hydrolysis leading to increased level of plasma lipid fractions (Yvore and Minguy,1972; Sharma and Fernando, 1973; Metwaly et al.,2013).Berberine has a strong potential to modulatehyperlipidemic status as seen from lowering serum triglyceride, cholesterol and LDLc levels and increasing the HDLc level (Leng et al., 2004; Punitha et al., 2004). It exerts its action via different mechanisms. It can inhibit pancreatic lipase activity (Mohammad et al., 2012). Berberine also can acts via stabilization of hepatic LDLc receptor (LDLR) and increasing transcriptional activity of LDLR promoter and down regulation of many transcription factors related to lipogenesis prCesses (Kong et al., adipogenic enzymes and transcription factors (Choi et al., 2006). Centrally administered berberine can stimulate muscular and hepatic AMPK activity and fatty acid oxidation and thereby contributing to improve lipid metabolism and systemic insulin sensitivity (Kim et al., 2006) and inhibit cholesterol and triglyceride synthesis (Yin et al., 2008). Moreover, berberine downregulated the expression of genes involved in lipogenesis and upregulated those involved in energy expenditure in adipose tissue and muscle (Lee et al., 2006).Intestinal E. papillata infection also induced a disturbance in both carbohydrate and protein status as revealed by the increased plasma glucose, total proteins and albumin levels with mutual decrease in jejunal carbohydrate and soluble protein contents. Berberine showed a hypoglycemic effect as it reduced blood glucose level and restored jejunal carbohydrate content. In spite of plasma total proteins and albumin were not increased significantly, but jejunal soluble protein content was significantly elevated.It was found that host cell metabolism is themost affected prCess during the intestinal bimerian infections (Al-Quraishy et al., 2012; Lutz et al.,2011) and these parasites have a great capacity to manipulate host cells for their benefits via scavenging available nutrients and essential host cell molecules (Forst, 2006; Hermosilla et al., 2012).Enhanced glycogenolysis andgluconeogenesis prCesses leads to breakdown of tissue carbohydrate store (Mondal et al., 2011; Metwaly et al., 2013) and hence increased blood glucose levels. Intestinal cCcidial infections have been classified as protein loosing enteropathy (Kouwenhoven, 1971). Many studies proved that there is decreased amount of total proteins in the infected tissues and increased rate of protein escape into the intestinal lumen via the ruptured intestinal wall assCiated with reduced absorption of amino acids and decreased digestibility of protein (Bangoura and Daugscies, 2007).Treatment with berberine was found to significantly decrease the catalytic prCesses of tissue protein and nucleic acid degradation (Punitha et al., 2004). Berberine was demonstrated to have a strong glucose lowering effects. It exerts itssecretion and/or action (Leng et al., 2004) or throughout extrapancreatic mechanisms independent of insulin secretion via either activation of glycolysis prCess or glycogenesis and/ or inhibition of gluconeogenesis (Punitha et al., 2004). Also, it has a strong potential to restore glucokinase activity and inhibit lipogenesis resulting in activation of glycolysis. Berberine reduced glucose-6- phosphatase enzyme activity which probably resulted in restoration of tissue glycogen content (Lee et al., 2006). In addition, treatment with berberine enhanced insulin-mediated glycogen synthesis and restored insulin inhibition of triglyceride secretion (Lou et al., 2011) and suppressing disaccharidase activities (Liu et al.,2010).Our data showed that E. papillata infection caused an increase in plasma levels of sodium and potassium, and a decrease in plasma selenium and ferrous ion concentrations. Again, berberine treatment reduced the increase in these metal ions and caused an increase in Se and Fe ion concentrations.The main reason for the disturbance in blood metal ion concentration is the produced diarrhoea by such infection which accompanied by severe loss of water and electrolytes within faeces (Coudret et al.,1988) in addition to decreased absorbability of the damaged intestine by E. Papillata. Diarrhoea leads to disrupted plasma concentrations of metal ions and changes in the mineral composition of the gut (Cirak et al., 2004; Bangoura and Daugscies, 2007). Also, Ghanem and Abdel Raouf (2005) and Gilbert et al. (2011) reported that metal ions are altered in their absorption due to the suppressed appetite and intestinal mucosal destruction which leads to malabsorption and altered ion transporters.Berberine was found to have a strong antidiarrheal activity as it could arrest diarrhea or reduce volume and frequency of diarrheal stool and their duration (Dutta et al., 1972; Khin et al., 1985). Its action Ccurs via depression of intestinal peristalsis and removal of inflammatory congestion of the mucosal surface of the intestine (Dutta et al.,1972; Khin et al., 1985). In addition, it is effective against the induced diarrhoea by several entero pathogenic bacteria as Vibrio cholera, Shigella, Pseudomonas, Escherichia coli and Proteus,parasites (Subbiah and Amin, 1967). It exerts its anti-secretory action via acting directly upon epithelial cells throughout blCkage of potassium and calcium ion channels (Taylor et al., 1999; Wang et al., 2004). In addition, berberine is a non- selective inhibitor of transepithelial ion transport across distal colonic mucosae via inhibition of basolateral potassium channel opening which would result in attenuation of the chloride secretory response (Taylor and Baird, 1995).Collectively, our data indicates that treatment of infected mice with berberine chloride could effectively ameliorate the induced pathological changes in lipid, protein, carbohydrate and metal ion homeostasis by E. papillata infection.ACKNOWLEDGEMENT

The authors extend appreciations to the Deanship of Scientific Research at King Saud University for funding the work through the research group project No. RGP-VPP-002.

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Author:Al-Quraishy, Saleh; Sherif, Nour E.; Metwaly, Mahmoud S.; Dkhil, Mohamed A.
Publication:Pakistan Journal of Zoology
Article Type:Report
Geographic Code:9PAKI
Date:Apr 30, 2014
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