Effects of Cd exposure on water metabolism (Total Body Water, Water influx, Water efflux, and Water Turnover Rates (WTR)and urinary and plasma osmolalities ) in adult
1. Introduction
Body fluid regulation is highly diverse among different animals according to their phylogenic position and the ecological condition [1]. The maintenance of water homeostasis in arid and semi-arid rodent habitats is a critical body function to survive the continually changing environmental condition. The combined effects of anatomical adaptations, behavioural patterns and interactions between hormonal systems allow these small mammals to minimize energetic costs and to finely balance body fluids under a wide range of conditions [2-3]. This is made possible essentially, by homeostatic mechanisms that concentrate urine as an indicator of water regulation efficiency as well as an advantage for colonization and survival [4].
AVP or antidiuretic hormone (ADH), is known to be primarily involved in water absorption in the distal nephron of the kidney in mammals. This peptide is synthesized in the soma of hypothalamic magnocellular neurosecretory cells (MNCSs) located in supraoptic (SON) and paraventricular (PVN) nuclei. After water deprivation the axons MNCs project to the neurohypophysis, where Ca2+ dependent exocytosis in their nerve terminals causes the release of AVP in blood circulation. The small peptide is secreted by the neurohypophysis in response to increases in plasma osmolality. AVP effects on the renal tubule are mediated by hormone binding to V2 type basolateral receptors coupled trough Gs to adenylyl cyclase and activation of the cyclic adenosine monophosphate - Protein kinase A (cAMP-PKA )cascade[13]. The hydroosmotic action causes a dramatic increase in the osmotic water permeability of connecting cells, principal cells and inner medullary collecting duct cells. The result is highly concentrated urines produced in response to water restriction.
The success of rodent to survive harsh environment condition goes back to several years ago. However, these animals are faced to substantial anthropogenic threats due to the introduction of heavy metals in environment in the last decades. Cadmium (Cd), a nonessential heavy metal, is widely distributed in the environment due to its use in primary metal industries and phosphate fertilizers [15, 16]. Food and cigarette smoke are the biggest sources of Cd exposure for the general population [17].In humans, Cd exposure leads to a variety of adverse effects and contributes to the development of serious pathological conditions [18-19]linked to enhanced aging process as well as cancer [20-21].Cd produces also neurotoxicity with a complex pathology [22-23]. In animals, Cd was shown to be toxic to all tissues such as liver [24], reproductive organs including the placenta, testis and ovaries [17, 25]. Several studies in some industrial sites in Tunisia showed that some habitats of
2. Material and methods
2.1. Animals and housing conditions
All experiments were carried out on adult male of Muridae;
Animals were randomly selected and divided into four groups. Eight animals, the first goup was used as control (C). Water was given
For immunohistochemistry study, treatment period had lasted from eight days to two weeks. Each animal was put in a metabolic cage for eight days in order to collect feces and 24 h urine each day at the same time. Urine samples were collected on paraffin oil to prevent evaporation and measured in mL/day. Daily consumption of drinking water and food of each group were measured throughout the study. It was not possible to collect urine since the 10 days of dehydration.
All of the protocols were carried out in accordance with French standard ethical guidelines for laboratory animals (agreement 75-178, 5_16_2000).
2.2. Techniques
Body weight of each animal was determined throughout the experiment. Blood samples were collected from the infra-orbital sinus into heparinized hematocrit capillary tubes, immediately before the experimental period and eight days later. These samples were centrifuged at 1500 g x for 10 min in order to determine hematocrit. At the end of experimentation rodents were sacrificed by decapitation, and brain, kidneys and livers were immediately removed and weighed. The weight of organs (%) was calculated as g /100 g of body weight. Finally these organs were dried at 60° C and weighed for the determination of dry weight.
2.3. Determination of water fluxes
Water fluxes were determined by direct analysis following the principles described by Holleman and Dieterich [30]. Rates of water flux represent the loss of water via excretion and evaporation and the simultaneous input of water, via metabolic water production and pre-formed water via food and drink (Nagy and Costa 1980). Free water content of the food determined by drying to constant weight at 60 °C was 3 %. The metabolic water content was determined from carbohydrate, fat and protein composition [33]. Thus 1 g of given food contains 0.509 mL of water. The intact unshaven carcasses were sublimated to dryness. The difference between live and dry weight was taken as total body water (TBW).
After determining urine volume and feces weight, urine samples were frozen at -30 °C while the feces were dried for 72 h. Water efflux was calculated as the difference between the influx and total body water. Water fluxes are expressed in H2O mL per day. Finally these fluxes were normalized to the average body weights and expressed in kg-0.82. In small mammals an allometric relationship exists between the water efflux or influx and body weight (W) in kilograms, which is Fin=K.W 0.82 ([34-35], expressed as mL/day/100 g body weight.
2.4. Tissue preparation
2.5. Immunohistochemistry
Free-floating sections were pretreated for 20 min with 3 % hydrogen peroxide in PBS to quench endogenous peroxidase. They were then washed with PBS (3 x 10 min), preincubated for 90 min at room temperature in PBS containing 0.05 %. Triton X-100 and 3 % normal horse serum. Sections were incubated for 36 h at 4 °C with Mouse anti-AVP antibody (1: 5000 dilution).
After incubation, sections were rinsed extensively with PBS (four times, 15 min) and incubated for 1.5 h in a 1/100 dilution of biotin conjugated horse anti-goat antibody and other secondary antibodies. Texas Red conjugated rabbit anti-mouse antibody (1/200; dilution; Jackson ImmunoResearch). For amplification, we used tyramide signal amplification fluorescence system technology (NEN, Boston, MA, USA). For details see Banisadr et al. [36]. After washing, sections were mounted onto gelatin-coated slides in Vectashield (Vector) and observed on fluorescent microscope (BX61; Olympus, Melville, NY) and a connected image-acquisition software (Analysis) was used.
2.6. Statistical analysis
Data are shown as the mean ± SEM. All results were compared to control animals (C), as well as to the Cd-exposed animals (Cd). For all our experiment, a two-way ANOVA was used to analyze the differences between groups, followed by a Dunnett’s test with a threshold of significance of p < 0.05 and p < 0.01 to detect specific differences, using a statistical software package (XLSTAT version 2009.1.1).
3. Results
3.1. Body mass
During the eight days of experimentation, body mass doesn’t change significantly in the control group. Body weight loss represented 5.77 ± 0.05 % in
3.2. Relative weights of organs
Relative weight of liver in controls is an average of 0.05 ± 0.01. Cd exposure significantly altered the relative weight of liver (0.036 ± 0.01) following eight days of treatment. Water restriction had no effect on relative weight of liver as compared to control
Decrease in relative weight of liver was also observed in water-deprived group and simultaneously treated with Cd. No differences were found in relative kidney weights (6.8 ± 0.9) in all groups under all experimental conditions.
3.3. Food consumption
Consumption of food was expressed per 100 g of body weight. Control animals consumed an average of 4.5 g/day of food. There was a significant (p<0.01) decrease of food intake in the Cd-exposed group (2.54 ± 0.2 g daily). Food intake of the water deprived groups was similar to that of the controls. When water deprivation was combined with Cd exposure, the decrease in food intake became larger and statistically significant compared with both control (p<0.01) and Cd-exposed groups (p<0.05).
3.4. Hematocrit
After eight days of experimentation, hematocrit(44.32 ± 1.08 %) did not change significantly in any treatment condition as compared to day 1 ( Fig. 3).
3.5. Water metabolism
Water metabolism data are shown in Table 1.
Treatment | Initial body weight (g) | Total body water (mL) | Total body water (%W) | Water influx mL | Water efflux mL | Water influx ml Kg -0.82 d -1 | Water efflux mL.Kg-0.82 d -1 | WTR in (% body water d -1) | WTR out (% body water d -1) | Urinary osmolality mOs/kg H20 | Plasma osmolality (mOs/kg H20) |
Control | 117.44 ±3.66 | 62.97 ±2.55 | 55.79 ±2.74 | 10.90 ±3.63 | 10.27 ±3.66 | 63.83 ±22.70 | 60.16 ±22.79 | 17.36 ±6.44 | 16.37 ±6.43 | 1100 ± 2 | 307.6 ± 4.2 |
Cd-exposed Meriones | 134.41 ±19.37 | 61.09 ±5.28 | 48.38 ±5.87 | 10.04 ±3.08 | 9.34 ±3.04 | 50.50 ±11.12 | 47.11 ±11.53 | 15.51 ±4.55 | 14.43 ±4.52 | 1600 ± 1.9** | 332 ± 3 |
Deprived wa ter Meriones | 120.37 ±16.85 | 64.89 ±1.23 | 61.30 ±9.28 | ▴▴ ⃰⃰ ⃰ 2.17 ±0.23 | ▴▴ ⃰⃰ ⃰ 1.93 ±0.56 | ▴ ⃰⃰ ⃰ 12.48 ±1.27 | ▴ ⃰⃰ ⃰ 11.96 ±3.34 | ▴▴ ⃰⃰ ⃰ 3.18 ±1.06 | ▴▴ ⃰⃰ ⃰ 3.12 ±0.67 | ▴▴ ⃰⃰ ⃰ 1700 ±1.9 | 345 ± 3 |
Deprived water and Cd-exposed Meriones | 128.25 ±18.67 | 67.59 ±1.36 | 60.50 ±9.99 | ▴▴ ⃰⃰ ⃰ 1.73 ±0.50 | ▴▴ ⃰⃰ ⃰ 1.81 ±0.76 | ▴ ⃰⃰ ⃰ 9.32 ±2.11 | ▴ ⃰⃰ ⃰ 9.62 ±3.28 | ▴▴ ⃰⃰ ⃰ 2.45 ±0.73 | ▴▴ ⃰⃰ ⃰ 2.66 ±1.09 | ▴▴ ⃰⃰ ⃰ 1162 ±2 | 307.6 ± 4.2 |
Total body water content in control group was 55.79 ± 2.74 (expressed by % of body weight). Throughout the experiments, body water was not significantly altered in any group. In animals having free access to water, water enters throughmetabolic water production and pre-formed water via food and drink.
The value of water influx was 10.90 ± 3.63 ml/ 63.83 ± 22.79 ml.Kg-0.82.d-1.This water influx (Fin) was not significantly affected in the group treated with Cd in comparison to control group. The loss of water via excretion (urine and fecal) and evaporation was Fout =10.27 ± 3.66 ml/60.16 22.79 ml.kg-0.82.d-1. Water fluxes rate were equal (Fin = Fout). This indicates that animals were in water equilibrium.After, one week of Cd exposure, water flux rates were not significantly affected in the group treated with Cd in comparison to control group and water equilibrium was maintained throughout the experiment.
Following one week of dehydration, the water influx rates was significantly decreased from about 5 times in Meriones treated or not with Cd (p<0.01). Cd exposure may not affected the water intake during our experiment.
In spite variations in water intake in different experimental conditions, all animals were in water equilibrium where water influx (Fin) and efflux (Fout) rates were equal (Fin = Fout).
3.6. Distribution of immunohistochemical staining for AVP
In control
Similarly to what was observed for AVP immunostaining in deprived animals without Cd, AVP immunoreactivity is strongly increased in SONfollowing eight days of water restriction (Fig. 2E) and PVN (Fig. 2F) compared to controls animals respectively (Fig.2A) and (Fig.3A). The increase of AVP immunostaining became more important by prolonged experiment for two weeks respectively in SON (Fig. 2F) and PVN (Fig. 3F).
However, AVP immunostaining from deprived water animals in the presence of Cd was markedly and significantly lower in SON (Fig. 2G) than in deprived water animals but not treated with Cd for a week (Fig. 2C). This decrease of AVP immunostaining becomes more important following two weeks of treatment (Fig. 2H) in comparison in two weeks deprived water animals not treated with Cd (Fig. 2D). Similar effect of AVP depletion in SON was also observed in PVN in simultaneously deprived water group and Cd-exposed Meriones during eight days (Fig. 3G) and two weeks (Fig. 3H) in comparison to those eight days deprived water group and two weeks deprived water groups and not treated with Cd.
3.7. Effect of Cd on water metabolism
The urinary osmolality (UO) in the control
In spite of the variations in water metabolism, all animals were in water equilibrium, at the end of experimentation. All these results indicate that even under the most stringent conditions
In order to maintain physiological serum osmolality, water intake and water loss are finely balanced by
Interestingly, the ability of acute systemic dehydration to produce AVP in both SON and PVN in
The current study is the first to explore the potential impact of Cd exposure on the magnocellular neuroendocrine system responsible for hydromineral balance. In this paper, we shown an involvement of the hypothalamo-vasopressinergic system of AVP, wish plays a fundamental role in the maintenance of body fluid homeostasis, in the protective reactions of the organism during Cd exposure in
Most strikingly, vasopressin is recognized as circulating hormone. Its actions were essentially confined to peripheral organs. However, currently AVP have been shown to be released in the brain as chemical messengers. AVP, like many peptides, when released within the brain, plays an important role in social behaviour. In rats, AVP is implicated in paternal behaviors, such as grooming, crouching over and contacting pups. AVP is also important for partner preference and pair bonding, particularly for males in a variety of species. It has been shown that AVP has powerful influences on complex behaviours [71].Disruption of vasopressinergic system has been linked to several neurobehavioural disorders including prader-Willi syndrome, affective disorders, obsessive-compulsive disorder and polymorphisms of V1a vasopressin receptor have been linked to autism [72].
4. Conclusion
On the basis of the current study, we conclude that Cd exposure modifies the vasopressinergic neuronal system and provides information regarding the neurotoxicity risks that this element presents for mammals and human populations exposed to Cd even to low amounts without affecting directly water metabolism. We are currently trying to study the linkage between Cd exposure and water controlling behavior at different level of the central nervous system.
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