Users Online: 1184

Home Print this page Email this page Small font sizeDefault font sizeIncrease font size

Home | About us | Editorial board | Search | Ahead of print | Current issue | Archives | Submit article | Instructions | Subscribe | Contacts | Login 
     

   Table of Contents      
ORIGINAL ARTICLE
Year : 2012  |  Volume : 2  |  Issue : 3  |  Page : 251-257

Monosodium glutamate modulates the circadian rhythms of biochemical variables and behavioral activity in rats under constant light


1 Department of Biotechnology, Faculty of Science, Vysya College, Salem, India
2 Department of Chemistry, Velammal Engineering College, Velammal Nagar, Ambattur-Red Hills Road, Chennai, India
3 Department of Biotechnology, Faculty of Science, Periyar University, Salem, India
4 Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University, Tamilnadu, India

Date of Web Publication8-Aug-2012

Correspondence Address:
Perumal Subramanian
Department of Biochemistry and Biotechnology, Faculty of Science, Annamalai University, Annamalainagar - 608 002, Tamil Nadu
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2231-0738.99479

Rights and Permissions
   Abstract 

Introduction: Suprachiasmatic nuclei (SCN) contained a variety of neurotransmitters and neuropeptides, and many of them could influence the activities of the circadian pacemaker. Glutamate was the major excitatory neurotransmitter in the mammalian central nervous system (CNS) and in SCN. Materials and Methods: Monosodium glutamate (MSG) (50 mg / kg body weight) was administered subcutaneously for 60 days to Wistar rats; open-field behavioral activity and 24-hour rhythms of glucose, cholesterol, total protein, phospholipids, aspartate transaminase (AST), and alkaline phosphatase (ALT) were studied under conditions of constant light (LL). Results: An open-field behavioral test showed that peripheral movement, central movement, rearing and grooming, were significantly decreased in LL, MSG and LL (MSG-treated) rats when compared with the control rats . The study revealed that the acrophase, amplitude, and mesor values of the glucose, protein, lipid profile, and liver marker enzymes of these rhythms were found to be altered in the experimental group rats when compared with the control rats. Conclusion: Monosodium glutamate, under constant light, modulated the circadian rhythms of lipid profiles and liver marker enzymes, which could be due to glutamate conveying the photic information to the SCN.

Keywords: Circadian rhythm, constant light, monosodium glutamate, suprachiasmatic nucleus


How to cite this article:
Kumaravel P, Subash S, Seethalakshmi KS, Murugan N, Yuvarajan R, Subramanian P. Monosodium glutamate modulates the circadian rhythms of biochemical variables and behavioral activity in rats under constant light. Int J Nutr Pharmacol Neurol Dis 2012;2:251-7

How to cite this URL:
Kumaravel P, Subash S, Seethalakshmi KS, Murugan N, Yuvarajan R, Subramanian P. Monosodium glutamate modulates the circadian rhythms of biochemical variables and behavioral activity in rats under constant light. Int J Nutr Pharmacol Neurol Dis [serial online] 2012 [cited 2019 Nov 16];2:251-7. Available from: http://www.ijnpnd.com/text.asp?2012/2/3/251/99479


   Introduction Top


The circadian clock is an evolutionary, highly conserved feature of bacteria, plants, and animals that allows organisms to adapt their physiological processes to the time of day in an anticipatory fashion. [1],[2] This internal timing mechanism coordinates the biochemical, physiological, and behavioral processes, to maintain synchrony with the environmental cycles of light, temperature, and nutrients. Circadian rhythms reflect the extensive programming of biological activities that meet and exploit the challenges and opportunities offered by the periodic nature of the environment. [2]

In mammals, circadian rhythms are driven by a timing system comprised of a master pacemaker in the SCN of the hypothalamus and peripheral oscillators located throughout the organism. Independent circadian oscillators exist within each cell of almost every tissue and / or organ investigated, including the liver and heart. [3],[4] The SCN adjusts its phase in response to this photic and nonphotic input, thereby maintaining its synchronization with the external world, by communicating the phase information to oscillators in tissues elsewhere in the brain, and in nearly all other tissues. [5]

Light is the most relevant cue for circadian entrainment, although nonphotic stimuli also function as zeitgebers or time givers. [6],[7] More recently, epidemiological studies have cited associational evidence that night shift work and exposure to light at night are risk factors for breast cancer. [8],[9] The suppression of melatonin by light exposure during shifts extending over the usual hours of nighttime darkness, have been postulated, and are supported by some experimental evidence in animals. [10] Constant light (LL) causes the release of glutamate, which initiates a signal transduction cascade in the SCN neurons that ultimately results in a phase shift of the circadian system. [11] Continuous exposure of bright light strongly suppresses the circadian rhythms of the sleep-wake cycle, drinking, locomotion, and body temperature. [12] Behavioral arousal or activation as well as the emotionality elicited by a novel environment is frequently analyzed by the open-field procedure. Behavioral arousal can be quantified by exploratory behaviors such as sniffing, walking, and rearing. [13],[14]

Monosodium glutamate is the sodium salt of an amino acid, glutamic acid. It has another name ajinomoto. It is used as a food additive, which causes only minor alterations in adults. Glutamic acid is one of the most abundant amino acids found in nature and exists as a free glutamate. [15] Glutamate is a major excitatory neurotransmitter in the brain and the most abundant amino acid in our daily diet. Excitatory action may, however, also lead to toxic effects related to excessive accumulation of extracellular glutamate. [16],[17] In vivo concentration of both the excitatory amino acid aspartate and glutamate have been seen to be higher during the dark phase than during the light phase in the rat SCN, in the LD (light-dark) cycle, and these are the major stimulatory neurotransmitters in the mammalian nervous system. [18] Glutamate in high doses produces neuroendocrine abnormalities, [19] neurodegeneration, neurotoxicity, [20] and oxidative damage in different organs. [21],[22]


   Materials and Methods Top


Adult male Wistar rats (180 - 200 g) were obtained from the Central Animal House, Faculty of Medicine, Annamalai University. The rats were housed in polypropylene cages at room temperature (30 ± 2° C) under semi-natural conditions. [23] The animals were maintained in natural light-dark cycles (12 : 12 hours) in an experimental room, under natural conditions. [24] All the animals were fed with the standard pellet diet (Hindustan Lever Ltd., Bangalore, India) and water was available ad libitum. Food and water were replenished daily. The experimental protocol was approved by the Committee for Research and Animal Ethics, Annamalai University (Vide No: 587/2008) and were in accordance with the guidelines of the National Institute of Nutrition (NIN), Indian Council of Medical Research (ICMR), Hyderabad, India.

The animals were randomized and divided into four groups (n = 6 in each group). MSG (50 mg / kg) was injected subcutaneously in group III and group IV rats, once a day, for 60 days. MSG was obtained from Himedia, Mumbai, India. Group - I Control (LD 12:12), Group - II Constant light (LL), Group- III MSG administration (50 mg / kg, subcutaneously), Group - IV Constant light condition + MSG administration (50 mg / kg, subcutaneously).

Open-field behavior is a simple test to evaluate the status of the animal by placing the animal in a brightly lit rectangular box (100 x 100 cm) with 40 cm height, made with walls of plywood. The floor consists of a clean plastic material painted in black dividing the field into 25 (5 x 5) equal squares. The rats are placed in the corner of the rectangular box and their behavior is observed for five minutes. This elicits a series of behavior-like peripheral and central movements and motor activity like grooming and rearing, related to the emotional status of the animal. [25]

After the experimental period, blood samples were collected after every four hours from each group of experimental and control rats (00:00, 04:00, 08:00, 12:00, 16:00, 20:00 and 24:00 hours) throughout the 24-hour period continuously. Minimal amount of blood was collected from the orbital sinus, with great care, using heparinized tubes. [26] Blood glucose was determined by using the O-toluidine method of Fings et al. [27] Briefly, 0.1 ml of blood was precipitated with 1.9 ml of 10% trichloro acetic acid (TCA), and the precipitate was removed after centrifugation. Next, 1 ml of supernatant was mixed with 4 ml of O-toluidine reagent and kept in a boiling water bath for eight minutes and cooled. The absorbance was read at 640 nm. Glucose was expressed as milligrams per deciliter of blood. Plasma cholesterol was estimated by the method of Zak et al. [28] Plasma of 0.1 ml and 4.9 ml of ferric chloride acetic acid reagent were mixed well and allowed to stand for 15 minutes to flocculate. Centrifuged and 3 ml of sulfuric acid was added to the supernatant. The chlolesterol in acetic acid gave a purple color with ferric chloride and sulfuric acid; the color developed was read at 560 nm.

Subsequently, the protein in the enzyme extract was determined using the method of Lowry et al. [29] The CO-NH group (peptide bond) present in the protein molecule reacted with the copper sulfate in the alkaline medium to give a blue color, which was read at 620 nm. Phospolipids in the serum were estimated by the method of Zilversmit et al. [30] This involved the conversion of organic phosphorus to inorganic phosphorus, which reacted with the ammonium molybdate to form phosphomolybdic acid. This on treatment with amino naphthol sulfonic acid (ANSA) formed a stable blue color, which was read at 680 nm.

The activities of AST were assayed by the method of Reitman and Frankel. [31] A 0.2 ml aliquot of serum with 1 ml of substrate (aspartate and α-ketoglutarate (KG) in phosphate buffer (pH 7.4)) was incubated for one hour. A 1 ml aliquot of 2,4-dinitrophenylhydrazine (DNPH) solution was added to arrest the reaction, and kept for 20 minutes at 25°C. After incubation, 1 ml of 0.4 N NaOH was added and the absorbance was read at 540 nm. The activities were expressed as IU / L. The ALP was assayed by the method of King and Armstrong. [32] The ALP activity was assayed using disodium phenylphosphate as a substrate. After preincubation of the buffer (0.1 M bicarbonate buffer, pH 10) with the substrate for 10 minutes, 0.2 ml of serum was added and incubated for 15 minutes at 25°C. The liberated phenols from the substrate reacted with a Folin-Phenol reagent (1 ml). The suspension was centrifuged and collected as the supernatant. An aliquot of 10% sodium bicarbonate 2 ml was added to the supernatant and the color that developed was read at 680 nm after 10 minutes. Activities of the ALP were expressed as IU / L.

The values of the variables (mean ± SD) were plotted versus the time of blood collection. Measurements of the acrophase (φ - measure of the peak time of the variable studied), amplitude (A - corresponded to half the total rhythmic variability in a cycle), mesor (M - rhythm adjusted mean), and 'r' values were calculated by the cosinor analysis using the 'cosinorwin' computer software program. [23]

Yti = M + A Cos (ωt - φ)

Where, Yti - Cosine function at the time point, M - Mesor, A - Amplitude, t - Time, φ - Phase.


   Results Top


The glutamate level was found to be increased in the brain tissues of group II animals (15.56 ± 0.18 μ mole / g tissue) and group IV animals (13.23 ± 0.78 μ mole / g tissue) compared to the control animals. However, there was no alteration in the levels of LL (MSG-treated rats). [Figure 1] shows the open-field behavioral activity as a peripheral movement where central movement, grooming, and rearing were significantly decreased in groups II, III, and IV, when compared with the control rats.
Figure 1: Open-field behavioral activity of Peripheral movement, Central movement, Grooming, and Rearing in control and experimental rats. Values are given as mean ± S.D from six rats in each group. Values not sharing a common superscript differ significantly at P < 0.05 (DMRT).

Click here to view


The biochemical variables measured in this study showed marked fluctuations over a 24-hour period in all the groups. The characteristics of rhythm with the r and p values indicated a detectable rhythmicity or non-significant temporal variation over a 24-hour period. The acrophase of the circadian rhythm of glucose was found at 00:32 hours in group I rats; in the case of group II, group III, and group IV rats maximum glucose levels were found at 22:57, 01:33, and 02:10 hours, respectively [Table 1]. The significantly increased mesor and decreased amplitude values were seen in groups II, III, IV rats, when compared with group I rats. Cholesterol activity showed peaking at 18:27 hours in normal and at 17:59 hours in MSG-treated rats, respectively. Acrophase was delayed in groups III and IV when compared to control rats. Increased mesor was found in groups III and IV, whereas, group II animals show decreased mesor values when compared to control rats, as shown in [Table 1].
Table 1: Temporal variation of glucose, cholesterol, and total protein in control and experimental rats

Click here to view


Peak activities of total protein were found during 07:29 and 08:10 hours in normal and MSG-treated rats, respectively. The acrophase was advanced in groups III and IV and a delay in group II, when compared to group I rats [Table 1]. The level of phospholipid was found to be at the peak at 11:18 hours in group I rats and maximum value of phospholipid in groups II, III, and IV rats was seen at 02:48, 09:55, and 12:12 hours, respectively. The amplitude and mesor values were altered significantly in groups ii, iii, 0 and IV, when compared with group I rats [Table 2]. Acrophase of AST activity revealed maximum activity in group I animals at 23:19 hours and in groups ii0 , III, and IV animals at 17:32, 02:43, and 21:17 hours, respectively. Increased mesor values were seen in groups II, III, and IV rats when compared with group I rats. The significant temporal variations of ALP over the 24-hour period. The acrophase of ALP was delayed in groups II, III, and IV, when compared to group I rats. The mesor value was increased in groups III and IV and decreased in group II, when compared to group I rats, as shown in [Table 2].
Table 2: Rhythmic pattern of Phospholipid, AST and ALP in control and experimental rats

Click here to view



   Discussion Top


Open-field behavioral test revealed that peripheral movement, central movement, rearing, and grooming, were significantly decreased in LL, MSG, and LL (MSG-treated) rats, when compared with control rats. LL-induced changes in circadian behaviour paralleled changes in the neuronal discharge of the SCN wherein high neuronal discharge occurred when locomotor activity was at its minimal level. [33] MSG or hypertonic saline treatment resulted in decreased intensity of locomotor activity, and a slow down of its uninterrupted habituation in the open-field test was observed in adult male rats. Reduced behavioral (locomotor) activities in MSG-treated rats might be due to excess activation of NMDA receptor cause lipid peroxidation in the brain and tissues. In LL-exposed and LL (MSG-treated) rats reduced locomotor activities were seen, which might be due to the (i) changes in the levels of acetylcholine and also modified cortisol, serotonin, GABA, and NPY in rat SCN, (ii) increased lipid peroxidation, (iii) modulates the pituitary and pineal glands, which leads to neuroendocrine hormonal level changes such as, melatonin, norepinephrine, and so on. [34],[35],[36],[37]

The peak and nadir values of glucose over a 24-hour period are well correlated with the temporal pattern of food intake, digestion, and accumulation of glucose in blood, [38] with the pervious reports demonstrating peak activity of glycolytic enzymes [39] during the night. Elevated levels of glucose in group II treated rats is due to increased peroxidation of lipids in red blood cells yielding free radicals. [40] Increased mesor of glucose in groups II and IV rats may be due to constant light, which can cause elevated catecholamines and / or corticosterone from the adrenal gland [41] and a peak level of glucagons. [42]

In addition free cholesterol of plasma low-density lipoproteins and high-density lipoproteins of the rats were high during the dark period. [43] Increased mesor of cholesterol in groups I i0 and IV might be due to the elevated lipid contents, which resulted in increased peroxidation in red blood cells. [40] LL caused elevated levels of corticosterone leading to decreased cholesterol synthesis, [44] this could be the reason for decreased amplitude and mesor values of cholesterol in group II rats. In rats, the rate-limiting enzyme (HMG CoA reductase) activity was shown to be high, [45, 46] and those of cholesterol biosynthesis precursors such as squalene and lanosterol were found to be higher [43] at midnight. LL caused elevated levels of corticosterone leading to decreased cholesterol synthesis. [44] This could be the reason for decreased amplitude and mesor values of cholesterol in group II rats.

The present study showed the peak time of total protein at 07:29 hours in group I rats; which corroborated with the previous reports. [47] Total protein rhythmicity was mainly attributed to the positive and negative balance between synthesis and degradation of protein. [48] Decreased mesor of total protein rhythm in groups II and IV, due to continuous light, caused restricted food access and acted directly upon the overt rhythm, without affecting the circadian oscillator. [49] A circadian rhythm of the content of total and individual phospholipids was found in the albino rat liver by biochemical methods. The phospholipid content and enzyme activity were higher during the daytime, 09:00 to 15:00 hours. The level of phospholipid was found to be at the peak at 11:18 hours in normal rats, which was corroborating with the previous reports. [50] The amplitude and mesor values were altered significantly in groups ii, iii, 0 and IV, when compared with group I rats.

The diurnal rhythms of many enzymes, including lactate dehydrogenase, aspartate transaminase, alanine transaminase, alkaline phosphatase, and acid phosphatase were well-documented. [51] Increased ALP activity in neonatal MSG-treated rats suggested that despite sustained hypophagia, their increased body fat content could also be caused by changes in the intestinal function. [52] The diurnal rhythms of plasma alkaline phosphatase were well-established in Wistar rats, the rhythms of ALP were not affected by the activity status of the animal, but they were synchronized by the environment factors like LD cycles. [23] Increased AST activity in the serum was generally accepted as an index of liver damage. [53] It was generally believed that one of the most important functions of AST was to transport reducing equivalents from cytosolically reduced NAD into the mitochondria by the 'malate-aspartate shuttle,' for production of energy. AST catalyzed the reversible transamination between aspartate and 2-oxoglutarate, to yield glutamate and oxaloacetate. [54]

Glutamate levels in the brain were increased in MSG-treated rats when compared to control rats. MSG administration did increase the glutamate levels within the arcuate nucleus dialysates, and plasma glutamate might be involved in the regulation of the blood brain barrier (BBB) permeability. [55] When the glutamate receptors, which were also demonstrated in cerebral capillaries, were overstimulated, a breakdown of the BBB could occur. [56],[57] A high dose of glutamate, particularly in young rats, was found to induce convulsions leading to increased cerebrovascular permeability. [58] Acute and chronic intake of relatively high doses of MSG, in adult rats, on the extracellular glutamate levels were altered in the hippocampus and hypothalamus, two brain areas particularly susceptible to glutamate-induced neurotoxicity. [59]


   Conclusion Top


The present study concludes that the administration of MSG under constant light treatment was found to cause acrophase delays in the glucose, phospholipid, aspartate transaminase rhythms, and advances in acrophases of cholesterol, alkaline phosphatase, and total protein levels. Glutamate levels in the brain were found to be significantly increased, which could alter these biochemical rhythms by modulating transmission in the retinohypothalamic tract and in the hypothalamic nuclei, probably including suprachiasmatic nuclei.

However, to elucidate the mechanisms, further research on neuroendocrine rhythms is needed.

 
   References Top

1.Daan S, Aschoff J. Circadian contribution to survival. In: Aschoff J, Daan S, Groos G, editors. Vertebrate Circadian System. Berlin: Springer-Verlag; 1982. p. 305-21.  Back to cited text no. 1
    
2.Pittendrigh CS. Temporal organization: Reflections of a Darwinian clock-watcher. Annu Rev Physiol 1993;55:16-54.  Back to cited text no. 2
[PUBMED]    
3.Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M. et al. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000;288:682-5.  Back to cited text no. 3
    
4.Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, et al. Period2: Luciferase real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 2004;101:5339-6.  Back to cited text no. 4
[PUBMED]    
5.Sloan MA, Levenson J, Tran Q, Kerbeshian M, Block GD, Eskin A. Aging affects the ocular circadian pacemaker of Aplysia californica. J Biol Rhythms 1999;14:151-9.  Back to cited text no. 5
[PUBMED]    
6.Mistlberger RE. Effects of scheduled food and water access on circadian rhythms of hamsters in constant light, dark, and light: Dark. Physiol Behav 1993;53:509-16.  Back to cited text no. 6
[PUBMED]    
7.Stephan FK. Interaction between light- and feeding-entrainable circadian rhythms in the rat. Physiol Behav 1986;38:127-33.  Back to cited text no. 7
[PUBMED]    
8.Anisimov VN. The role of pineal gland in breast cancer development. Crit Rev Oncol Hematol 2003;46:221-34.  Back to cited text no. 8
[PUBMED]    
9.Jasser SA, Blask DE, Brainard GC. Light during darkness and cancer: Relationships in circadian photoreception and tumor biology. Cancer Causes Control 2006;17:515-23.  Back to cited text no. 9
[PUBMED]    
10.Blask DE, Dauchy RT, Sauer LA, Krause JA, Brainerd GC. Light during darkness, melatonin suppression and cancer progression. Neuroendocrinol Lett 2002;23:52-6.  Back to cited text no. 10
    
11.Golombek DA, Ferresyara GA, Agostino PV, Murad AD, Rubio MF, Pizzio GA, et al. From light to genes: Moving the hands of the circadian clock. Front Biosci 2003;8:56-70.  Back to cited text no. 11
    
12.Depres-Brummer P, Levi F, Metzger G, Touitou Y. Light-induced suppression of the rat circadian system. Am J Physiol 1995;268:1111-6.  Back to cited text no. 12
    
13.Crussio WE, Schwegler H, Van abeelen JH. Behavioral response to novelty and structural variation of the hippocampus in mice. II. Multivariate genetic analysis. Behav Brain Res 1989;32:81-8.  Back to cited text no. 13
    
14.Cerbone A, Sadile AG. Behavioral habituation to spatial novelty: Interference and noninterference studies. Neurosci Behav Rev 1994;18:497-518.  Back to cited text no. 14
[PUBMED]    
15.Giacometti T. Free and bound glutamate in natural products. In: Glutamic Acid: Advances in Biochemistry (Filer LJ, Garattini S, Kare MR, Reynolds WA, Wurtman RJ, editors). New York: Raven Press; 1979. p. 25-34.  Back to cited text no. 15
    
16.Beal MF. Mechanisms of excitotoxicity in neurologic diseases. FASEB J 1992;6:3338-44.  Back to cited text no. 16
[PUBMED]    
17.Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS. Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 1992;2:431-5.  Back to cited text no. 17
[PUBMED]    
18.Honma S, Katsuno Y, Shinohara K, Abe H, Ichi-Honma K. Circadian rhythm and response to light of extracellular glutamate and aspartate in rat suporachiasmatic nucleus. Am J Physiol 1996;271:R579-85.  Back to cited text no. 18
    
19.Moreno G, Perello M, Gaillard, RC, Spinedi, E. Orexin a stimulates hypothalamic pituitary adrenal (HPA) axis function, but not food intake, in the absence of full hypothalamic NPY-ergic activity. Endocrine 2005;26:99-106.  Back to cited text no. 19
    
20.Chaparro-Huerta V, Rivera-Cervantes MC, Torres-Mendoza BM, Beas-Zárate C. Neuronal death and tumour necrosis factor- alpha response to glutamate induced excitotoxicity in the cerebral cortex of neonatal rats. Neurosci Lett 2002;333:95-8.  Back to cited text no. 20
    
21.Farmobi EO, Onyema OO. Monosodium glutamate induced oxidative damage and genotoxicity in the rat. Modulation role of vitamin C, vitamin E and quercetin. Hum Exp Toxicol 2006;25:251-9.  Back to cited text no. 21
    
22.Pavlovic V, Pavlovic D, Kocic G, Sokolovic D, Jevtovic-stoimenov T. Effect of monosodium glutamate on oxidative states and apoptosis in rat thymus. Mol Cell Biochem 2007;303:161-6.  Back to cited text no. 22
    
23.Manivasagam T, Subramanian P. Influence of monosodium glutamate on circadian rhythms of lipid peroxidation products and antioxidants in rats. Italian J Pharmacol 2004;53:72-6.  Back to cited text no. 23
[PUBMED]    
24.Subash S, Subramanian P. Effect of N- phthaloyl gamma aminobutyric acid on lipid Peroxidation, antioxidants and liver markers in constant light exposed rats. Int J Nutr PharmacolNeurol Dis 2011;1:163-6.  Back to cited text no. 24
    
25.Rajashankar S, Manivasagam T, Surendran S. Ashwaganda leaf extract: A potential agent in treating oxidative damage and physiologicall abnormalities seen in a mouse model of parkinson's disease. Neuroscience Lett 2009;25868:1-5.  Back to cited text no. 25
    
26.Subramanian P, Sivabalan S, Menon VP, Vasudevan K. Influence of chronic zinc supplementation on biochemical variables and circadian rhythms in Wistar rats. Nutr Res 2000;20:413-25.  Back to cited text no. 26
    
27.Fings CS, Toltiff C r0 , Duonin RJ. Glucose determination by O-toludine method using glacial acetic acid In: Practical clinical chemistry. Toro G, Ackermann PG, editors. New York: Little Brown and company; 1970. p. 115-8.  Back to cited text no. 27
    
28.Zak B, Boyle AJ, Zaltkis A. A method for the direct determination of serum cholesterol. J Clin Med 1953;45:486-92.  Back to cited text no. 28
    
29.Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin-phenol reagent. J Biol Chem 1951;193:265-75.  Back to cited text no. 29
[PUBMED]    
30.Zilversmit DB, McChandless EL, Davis AK. Microdetermination of plasma phospholipids by trichloroacetic acid precipitation. J Lab Clin Med 1950;35:155.  Back to cited text no. 30
    
31.Reitman S, Frankel AS. A colorimetric method for the determination of serum glutamic, oxaloacetic and glutamic pyruvic transaminases. Am J Clin Path 1974;28:53-6.  Back to cited text no. 31
    
32.King EJ, Armstrong AR. Determination of serum and bile phosphatase activity. Canad Med Assoc J 1934 31:56-63.  Back to cited text no. 32
    
33.Rafnssion V, Tulinius H, Jonasson JG, Hrafnkelsson J. Risk of breast cancer in female flight attendants: A population based study (Iceland). Cancer Causes Control 2001;12:95-101.   Back to cited text no. 33
    
34.Kizer JS, Nemeroff CB, Youngblood WW. Neurotoxic aminoacids and structurally related analogs. Pharmacol Res 1978;29:301-8.  Back to cited text no. 34
    
35.Hlinak Z, Gandalovicova D, Krejci I. Behavioral deficits in adult rats treated neonatally with glutamate. Neurotoxicol Teratol 2005;27:465-73.  Back to cited text no. 35
    
36.Poon TK, Cameron DP. Measurement of oxygen consumption and locomotor activity in monosodium glutamate-induced obesity. Am J Physiol 1978;234: E532-4.  Back to cited text no. 36
[PUBMED]    
37.Subash P, Subramanian. Impact of morin (a bioflavonoid) on ammonium chloride-mediated oxidative damage in rat kidney. Int J Nutr Pharmacol Neurol Dis 2011;1:174-8.  Back to cited text no. 37
  Medknow Journal  
38.Subramanian P, Menon VP, Arockiam FV, Rajakrishnan V, Balamurugan E. Lithium modulates biochemicals circadian rhythms in Wistar rats. Chronobiol Int 1998;15:29-38.  Back to cited text no. 38
    
39.North C, Fevers RJ, Scheving LE, Pauly JE, Tsai TH, Casciano DA. Circadian organization of thirteen liver and six brain enzymes of mouse. Am J Anat 1981;162:183-99.  Back to cited text no. 39
    
40.Ahluwalia P, Tawari K, Choudhary P. Studies on the effects on monosodium gluatamate (MSG) on oxidative stress in erythrocytes of adult male mice. Toxicol Lett 1996;84:161-5.  Back to cited text no. 40
    
41.Challet E, Malan A, Turek WF, Van Reeth O. Daily variations of blood glucose, acid-base state and pCO 2 in rats: Effect of light exposure. Neurosci Lett 2004;355:131-5.  Back to cited text no. 41
    
42.Le Blanc J. Nutritional implications of cephalic phase thermogenic responses. Appetite 2000;34:214-6.  Back to cited text no. 42
    
43.Strandberg TE, Tilvis RS, Miettinen TA. Diurnal variation of plasma methyl sterols and cholesterol in the rat: Relation to hepatic cholesterol synthesis. Lipids 1984;19:202-5.  Back to cited text no. 43
[PUBMED]    
44.Ueberberg H, Laque K, Trieb G. Comparative studies on the circadian rhythm of corticosterone lipid and cholesterol levels in adrenals and blood of rats. Chronobiol Int 1984;1:41-9.  Back to cited text no. 44
    
45.Mietenen TA. Diurnal variation of cholesterol precusors squalene and methyl sterols in human plasma lipoproteins. J Lip Res 1982;23:466-73.  Back to cited text no. 45
    
46.Pappu AS, Illingworth DR. Diurnal variations in the plasma concentrations of mevalonic acid in patients with abeta lipoproteinaemia. Eur J Clin Invest 1994;24:98-702.  Back to cited text no. 46
[PUBMED]    
47.Rajasekar P, Subramanian P, Manivasagam T. Circadian variations of biochemical variables in aspartame treated rats. Pharmaceut Boil 2004;42:1-7.  Back to cited text no. 47
    
48.Touitou Y, Reinberg A, Bogdan A, Auzeby A, Beck H, Touitou C. Differences between young and elderly subjects in seasonal circadian variations of total plasma proteins and blood as reflected by hemoglobin, hematocrit and erythrocyte counts. Clin Chem 1989;321:801-4.  Back to cited text no. 48
    
49.Abe H, Kida M, Tsuli K, Mano T. Feeding cycle entrain circadian rhythms of locomotor activity in CS mice but not in C57 BL/6J mice. Physiol Behav 1989;45:397-402.  Back to cited text no. 49
    
50.Ginovker AG, Konovalova LA, Zhikhareva AI. Circadian rhythm of phospholipid content and nonspecific phosphomonoesterase activity in the rat liver. Bull Exp Bio Med 1979;88:1351-4.  Back to cited text no. 50
[PUBMED]    
51.Riversa-coll a0 , Fuentes-Arderiv X, Diez-Noguera A. Circadian rhythms of serum concentration of 12 enzymes of clinical interest. Chronobiol Int 1993;10:190-200.  Back to cited text no. 51
    
52.Martinkova A, Lanhardt L, Mozes S. Effect of neonatal MSG treatment on day-night alkaline phosphatase activity in the rat duodenum. Physiol Res 2000;49:339-45.  Back to cited text no. 52
    
53.Ha WS, Kim CK, Song SH, Kang CB. Study on mechanism of multistep hepatotumorigenesis in rat: Development of hepatotumorigenesis. J Vet Sci 2001;2:53-8.  Back to cited text no. 53
[PUBMED]    
54.Johnson JL. An analysis of the activities of 3 key enzymes concerned with the inter conversion of the á-ketoglutarate and glutamate: Correlations with free glutamate levels in the nervous system. Brain Res 1972;45:205-15.  Back to cited text no. 54
[PUBMED]    
55.Mayhan WG, Didion SP. Glutamate-induced disruption of the blood- brain barrier in rats. Role of nitric oxide. Stroke1996;27:965-70.  Back to cited text no. 55
    
56.Huang QF, Gebrewold A, Zhang A, Altura BT, Altura BM. Role of excitatory amino acids in regulation of rat pial microvasculature. Am J Physiol 1994;266:R158-63.  Back to cited text no. 56
    
57.Koenig H, Trout JJ, Goldstone AD, Lu CY. Capillary NMDA receptors regulate blood- brain barrier function and breakdown. Brain Res 1992;588:297-303.  Back to cited text no. 57
    
58.Nemeroff CB, Crisley FD. Monosodium L-glutamate-induced convulsions: Temporary alteration in blood- brain barrier permeability to plasma proteins. Environ Physiol Biochem 1975;5:389-95.  Back to cited text no. 58
    
59.Peng Y, Gubin J, Harper AE, Vavich MG, Kemmerer R. Food intake regulation: amino acid toxicity and changes in rat brain and plasma amino acids. J Nutr 1973;103:608-17.  Back to cited text no. 59
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2]


This article has been cited by
1 Ginger and Propolis Exert Neuroprotective Effects against Monosodium Glutamate-Induced Neurotoxicity in Rats
Usama Hussein,Nour Hassan,Manal Elhalwagy,Amr Zaki,Huda Abubakr,Kalyan Nagulapalli Venkata,Kyu Jang,Anupam Bishayee
Molecules. 2017; 22(11): 1928
[Pubmed] | [DOI]
2 Answer to letter sent by Dr. M.D. Rogers (Chairman of the International Glutamate Technical Committee (IGTC), Belgium) related to Ataseven et al. article published in Food and Chemical Toxicology 2016; 91:8–18
Fatma Unal,Nazmiye Ataseven,Ayten Celebi Keskin,Deniz Yuzbasioglu
Food and Chemical Toxicology. 2016;
[Pubmed] | [DOI]
3 The cyanobacteriumOscillatoria brevisß-carotene extract modulates alterations of biochemical and hematological circadian patterns in stress-induced rat
Menatallah M. Mohammed,Alaa E. Sallam,Aida A. Hussein,Diaa A. Marrez,Zohour N. Ibrahim
Biological Rhythm Research. 2015; : 1
[Pubmed] | [DOI]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed5546    
    Printed113    
    Emailed0    
    PDF Downloaded155    
    Comments [Add]    
    Cited by others 3    

Recommend this journal