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© 2006 American Society for Nutrition J. Nutr. 136:1256-1260, May 2006

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

A High-Protein, High-Fat, Carbohydrate-Free Diet Reduces Energy Intake, Hepatic Lipogenesis, and Adiposity in Rats

Lisa Pichon, Jean-François Huneau, Gilles Fromentin1 and Daniel Tomé

UMR INRA 914 Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon, F75231 PARIS Cedex 05, France

1 To whom correspondence should be addressed. E-mail: fromenti{at}inapg.fr.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The aim of this work was to determine the effects in rats of ingesting 1 of 3 diets with normal or high protein concentrations and various carbohydrate:lipid ratios on weight gain, body composition, and the development and metabolism of white adipose tissue (WAT). For this purpose, male Wistar rats were fed for 20 or 42 d a high-carbohydrate, low-fat, normal-protein diet (76, 10, and 14% of energy as carbohydrate, lipid, and protein, respectively, carbohydrate:lipid ratio (C/L) = 7.6), a normal-carbohydrate, low-fat, high-protein diet (35, 10, and 55% of energy as carbohydrate, lipid, and protein respectively, C:L = 3.5), or a carbohydrate-free, high-fat, high-protein diet (45 and 55% of energy as fat and protein, respectively, C:L = 0). Growth, food intake, body composition, WAT cellularity, and several markers of lipogenesis including fatty acid synthase and lipoprotein lipase activities were measured in adipose tissue and liver. Lowering the C:L ratio reduced the development of WAT, weight gain, body fat mass, and adipocyte size, and in rats fed the carbohydrate-free diet (C:L = 0), the total number of adipocytes in subcutaneous WAT. These reductions in adipose tissue development with decreases in the C:L ratio of the diet seemed to be due primarily to reduced hepatic lipogenesis.

KEY WORDS: • adipocytes • body composition • fatty acid synthase • lipoprotein lipase • carbohydrate-free diet

The precise role of different macronutrient combinations, i.e., the relative effects of carbohydrate, fat, and protein on total energy intake, energy metabolism, and adiposity, remains a subject of debate. Increasing the protein content in the diet usually reduces energy intake and fat deposition (1–5). Different studies also showed the importance of the carbohydrate to fat ratio rather than the fat content per se in the diet to the development of adiposity (6). In this context, a high-fat diet would lead to overfeeding and obesity when the diet is also rich in carbohydrate, which favors insulin secretion, lipogenesis, and fat deposition, whereas in the absence of carbohydrate, a lower insulin response to feeding would favor lipid oxidation rather than deposition. The present study addressed the effects of lowering the carbohydrate:lipid (C:L)2 ratio of the diet in a context of a normal or high-protein diet on energy intake, lipogenesis, and adiposity. For this purpose, energy intake, body weight gain, body composition, adipose tissue cellularity, lipogenesis in the liver [fatty acid synthase (FAS)] and lipolysis in the adipose tissue [lipoprotein lipase (LPL)] were determined in rats fed one of the following: 1) a control (high-carbohydrate, low-fat, normal-protein, i.e., a high C:L) diet, 2) a normal-carbohydrate, low-fat, high-protein, i.e., a normal C:L ratio diet obtained by increasing protein at the expense of carbohydrate without any change in the fat content, or 3) a carbohydrate-free, high-fat, high-protein, i.e., a 0 C:L ratio] diet obtained from situation 2 by increasing the level of fat at the expense of carbohydrate.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Animals and diets. Male Wistar rats were housed individually in stainless steel wire cages in a room with a 12-h light-dark cycle (lights on: 1030–2230) and maintained at a temperature of 21 ± 1°C. The rats were adapted for 10 d to a control diet providing an adequate intake of protein (14% total milk protein) and then switched to 1 of the 3 experimental diet (Table 1): the high-carbohydrate, low-fat, normal-protein group (P14C76L10) was fed a diet with 76% of energy as carbohydrate, 10% as fat, and 14% as protein. The normal-carbohydrate, low-fat, high-protein group (P55C35L10) was fed a diet providing 35% of energy as carbohydrate, 10% as fat, and 55% as protein, and the carbohydrate-free, high-fat, high-protein group (P55L45) was fed a diet devoid of carbohydrate, providing 45% of energy as fat and 55% as protein. Rats had free access to food and water, with fresh food provided daily. They consumed the experimental diets for 42 d in Expt. 1 (preliminary experiment) and for 20 d in Expt. 2.


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  		TABLE 1 Composition of the diets

 
In a preliminary experiment (Expt. 1), 24 Wistar rats, initially weighing 310 ± 5 g were acclimated and then divided into 3 groups as described above. Growth and food intake were measured on a daily basis for 42 d. In a second experiment (Expt. 2), 24 Wistar rats initially weighing 180 ± 5 g were acclimated and then divided into 3 groups as described above. On d 20, 8 rats from each group were killed for the determination of body composition, white adipose tissue (WAT) cellularity, and LPL and FAS activity. Blood samples were collected and plasma was stored at –80°C until analysis. Samples of retroperitoneal and subcutaneous WAT (4 g) were processed immediately to determine adipocyte cell size distribution and fat pad cellularity, and to measure triglyceride levels, as described below. All experiments were carried out in accordance with the recommendations of the French Committee for Animal Care.

    Adipocyte isolation and WAT cellularity assessment. Adipocyte isolation from retroperitoneal and subcutaneous white adipose fat pad was performed by collagenase digestion, according to the Rodbell method modified by Martinson (7). Briefly, 3 g of tissue were cut with a pair of scissors and added in 10 volumes of oxygenated (O2:CO2, 95:5) Krebs-Ringer buffer [120 mmol/L NaCl, 4.7 mmol/L KCl, 1.25 mmol/L CaCl2, 1.2 mmol/L KH2PO4, 1.2 mmol/L MgSO4·7H2O, 32.3 mmol/L NaHCO3, 4% bovine serum albumin (BSA), 5 mmol/L glucose, pH 7.4], and 10 mg collagenase was added per gram of WAT. Digestion was allowed to proceed at 37°C under mild agitation for 45 min in polypropylene tubes. Floating adipocytes were filtered through a 190-µm Nylon gauze, collected, rinsed in collagenase-free buffer, and diluted in 2.5 mmol/L Ca2+Krebs-Ringer buffer. The cell suspension (100 µL) was gently spotted onto a microscope slide and cell diameters were measured on 100 adipocytes using a micrometric scale (X40). Mean adipocyte volume was calculated according to the method described by Goldrick (8): V = {pi}/6 x d (d2 + 3{sigma}2), where d is the mean diameter and {sigma}2 is the variance of the diameter on 100 adipocytes. The amount of lipid per milligram fat pad was measured on a 1-g sample, using the method of Folch (9). Assuming a density of 0.915 for adipocytes, corresponding to that of a triolein droplet, the number of adipocytes per milligram of fat pad could be calculated, when the mean lipid content of one adipocyte was known.

    Adipose tissue lipoprotein lipase (LPL) activity. Lipoprotein lipase activity in retroperitoneal WAT was assessed using the method described by Nilsson-Ehle and Schotz (10); LPL was extracted as described by Dugail (11). Retroperitoneal tissue was crushed at 4°C in 50 mmol/L NH4Cl buffer, pH 8, containing 4% BSA and 4 kIU/L heparin. Proteins were precipitated with acetone, pelleted by centrifugation (3500 x g, 20 min, 4°C), rinsed 3 times with acetone, and dried with diethyl ether. Proteins were resuspended in 50 mmol/L NH4Cl, pH 8.1, containing 4 kIU/L heparin. Insoluble particles were removed by centrifugation (3500 x g, 20 min, 4°C) and the supernatant was used as a source of LPL. The substrate was prepared by mixing 1 volume of solution A [600 mg triolein trace-labeled with 150 µCi [3H]-triolein (2 TBq/mmol, NEN) and 36 mg egg lecithin dissolved in 10 mL glycerol], 4 volumes of 0.2 mol/L Tris HCl buffer pH 8.1 containing 150 mmol/L NaCl and 3% BSA, and 1 volume of heated rat serum as a source of apolipoprotein CII, the natural activator of LPL. The reaction was started by mixing 100 µL of substrate and 100 µL enzyme solution; it was allowed to proceed for 1 h at 37°C in a shaking water bath. The reaction was stopped by successively adding 3.5 mL of methanol:chloroform:heptane (141:125:100, by vol) and 1.05 mL potassium tetraborate:potassium carbonate buffer 0.1 mol/L, pH 10.5. After agitation and centrifugation (3000 x g, 4°C, 10 min), 1 mL of the methanol alkaline phase containing the free fatty acids was transferred to a scintillation flask and counted using liquid scintillation. Results were expressed as nanomoles of free fatty acids released per 100,000 cells per hour.

    Liver fatty acid synthase (FAS) activity. Liver FAS activity was assessed using the spectroscopic method described by Halestrap and Denton (12). The liver (500 mg) was homogenized at 4°C in 5 volumes of Tris HCl buffer, pH 7.4, containing 0.25 mol/L sucrose, 1 mmol/L dithiothreitol, and 1 mmol/L EDTA. The homogenate was centrifuged at 48,000 x g and 4°C for 2 h and the supernatant used as an enzyme source. The reaction took place at 37°C in 0.1 mol/L potassium phosphate buffer, pH 6.5, with 0.1 mmol/L NADPH,H+, 25 µmol/L acetyl CoA, and 60 µmol/L malonyl CoA. The oxidation of NADPH,H+ was monitored continuously by absorbance measurement at 340 nm. Proteins were assayed using the bicinchoninic acid method (13).

    Body composition. Carcass analysis was conducted on the rats remaining at the end of the 20-d feeding period. The rats were deprived of food overnight and killed with an i.p. injection of 13.6 mg/100 g body weight sodium pentobarbital (Sanofi santé animale). Blood samples were collected rapidly from the vena cava in heparinized syringes, to prevent clotting. The abdomen was then opened and the liver, the two main abdominal fat pads (epididymal and retroperitoneal), the subcutaneous fat pad, the interscapular BAT, and the stripped carcass were quickly removed and weighed.

    Statistical analysis. All results are expressed as means ± SEM. Body weight and food intake data were analyzed using the mixed procedure for repeated measurements in the SAS software package (SAS version 8.02), with group and time as fixed effects. Generalized linear model analysis was used for the comparison of body composition, FAS and LPL activity, and the size distribution of adipocytes was analyzed using the {chi}2 test.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    Food intake and body weight gain. In Expt. 1, growth and food intake were measured daily for 42 d in rats fed the P14C76L10, P55C35L10, or P55L45 diet. During the adaptation period (until d 0), rats (n = 24) consumed 409 ± 12 kJ/d and their mean body weight was 346 ± 5 g at the time of the introduction of the experimental diet. During the 42-d feeding period, rats fed the P14C76L10 diet consumed more energy than those fed the P55C35L10 or the P55L45 diets (group effect P < 0.05, time x group effect P < 0.001) (Fig. 1B. Overall, lowering the C:L ratio of the high-protein diet from 3.5 to 0 (P55C35L10 and P55L45 groups) did not affect energy intake (P = 0.58; P55C35L10 and P55L45), although a slight but significant reduction of energy intake occurred during the first 2 wk, followed by a gain during the subsequent period (time x group effect, P < 0.01). Compared with the P14C76L10 group, weight gain was lower in both the P55C35L10 and the P55L45 groups throughout the experimental period (group effect P < 0.05, group x time effect P < 0.01) (Fig. 1A). Growth was further decreased when the G:L ratio of the diet was lowered from 3.5 to 0 (group effect P < 0.05). The difference between the P55C35L10 and the P55L45 fed rats was significant after only 2 d of experimental diet and remained almost constant throughout the experiment (no group x time effect). In the next experiment (Expt. 2) which considered body composition, adipocyte cellularity, and enzymatic activities, the initial weight was lower. The rats were also fed the experimental diets for a shorter period (20 d), but body weight gain and food intake were similar (data not shown).


Figure 1
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  		FIGURE 1  Cumulative body weight (A) and energy intake (B) of rats consuming the P14C76L10, P55C35L10, or P55L45 diet ad libitum. Values are means ± SD, n = 8. Means without a common letter differ, P < 0.05.

 
    Body composition. Organ weight proportions at the end of the experiment differed as a function of diet (Table 2). Compared with the P14C76L10 group, all of the fat pads and the total WAT of the P55C35L10 group were not different. But when the adiposity index (AI, calculated by dividing total WAT weight by the weight of the stripped carcass) was compared, the reduction in the C:L ratio from 7.6 to 3.5 reduced adiposity because the AI was lower in the P55C35L10 than in the P14C76L10 group (P < 0.0005). Compared with the P14C76L10 and P55C35L10 groups, P55L45 rats had lower total body fat mass. This was also the case for each of the fat pads (epididymal, retroperitoneal, and subcutaneous), and the AI (P < 0.0075). Thus, reduction of the C:L ratio from 3.5 to 0 also reduced body fat mass. These effects of the C:L ratio of the diet were also observed for the proportion of scapular BAT. Lowering the C:L ratio in the diet led to an enhancement of the liver proportion.


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  		TABLE 2 Body weight and organ weights of rats after ad libitum consumption of the P14C76L10, P55C35L10, or P55L45 diet for 37 d1

 
    Adipose tissue cellularity. Cell size distributions in the retroperitoneal fat pad were similar to those of the subcutaneous WAT (Fig. 2). Compared with the P14C76L10 group, the adipocyte size distributions in the P55C35L10 and P55L45 groups were shifted toward smaller diameters in both retroperitoneal and subcutaneous tissues. This shift was more pronounced in the P55L45 group than in the P55C35L10 group because 53% of the adipocytes in the retroperitoneal fat pad and 60% in the subcutaneous fat pad were smaller than 100 µmol/L in the former group compared with 41 and 47% in the latter group. Consistently, the mean diameters of retroperitoneal and subcutaneous adipocytes were significantly higher in the P14C76L10 group than in the P55C35L10 and P55L45 groups (retroperitoneal: P < 0.0001; subcutaneous: P < 0.0006). The number of adipocytes in retroperitoneal tissue was significantly smaller in the P55L45 group (P < 0.0405) but did not differ in the P55C35L10 and P14C76L10 groups (Table 3). In subcutaneous tissue, the total number of adipocytes did not differ among the 3 groups. The cellularity (number of adipocytes/mg of tissue) of retroperitoneal and subcutaneous WAT differed significantly among the groups, with higher values in P55L45 rats and lower values in P14C76L10 rats.


Figure 2
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  		FIGURE 2  Adipocyte size distribution of retroperitoneal (A) and subcutaneous adipose tissue (B) of rats consuming the P14C76L10, P55C35L10, or P55L45 diet ad libitum. Values are means ± SD, n = 8. Distributions without a different letter differ P < 0.05.

 

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  		TABLE 3 Cellularity of retroperitoneal and subcutaneous adipose tissues of rats after ad libitum consumption of the P14C76L10, P55C35L10, or P55L45 diet for 37 d1

 
    Liver FAS and WAT LPL activities. Hepatic FAS activity was greater in rats fed P14C76L10 than in those fed P55C35L10, and it was greater in this group than in the group fed P55L45 (Table 4). LPL activity in WAT did not differ among the group.


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  		TABLE 4 Lipolysis and lipogenesis in liver and in retroperitoneal WAT, respectively, of rats after ad libitum consumption of the P14C76L10, P55C35L10, or P55L45 diet for 37 d1

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The purpose of this study was to evaluate the effects in rats of lowering the C:L ratio of the diet in the context of a normal or high-protein diet on energy intake, lipogenesis, and adiposity. Lowering the C:L ratio reduced energy intake, body weight gain, liver lipogenesis, adipocyte size, and fat deposition in adipose tissue, but did not modify the number of adipocytes, except in the case of the carbohydrate-free diet.

As shown previously, compared with a high-carbohydrate, normal-protein, low-fat diet (P14C76L10), rats fed a high-protein, low-fat diet (P55C35L10 group) (obtained by replacing protein for carbohydrate) had reduced energy intake (4). Indeed, proteins were shown previously to have the strongest appetite suppressive effect of the 3 macronutrients in animals and humans (14). This could explain the differences in food intake between the P14C76L10 group on the one hand and the P55C35L10 and P55L45 groups on the other hand. For weight gain and adiposity, the differences between groups could be due to several mechanisms that are interdependent. First, the diversion of amino acids to catabolic pathways and gluconeogenesis is thought to be associated with a stronger thermogenic effect of the diet, which induces a reduction in food efficiency, and consequently weight gain and adiposity (15). Indeed, higher food efficiency leads to fat storage. That could explain why rats fed P55C35L10 had a lower weight gain and less adiposity than the P14C56L30 group. To a further extent, the lower weight gain in the P55L45 group compared with the P55C35L10 group, despite their similar food intake, could also be due to a subsequent increase in gluconeogenic activity to compensate for the absence of carbohydrate from the diet. These results show that in fact, the carbohydrate content in the diet, which determines the level of gluconeogenic activity, is directly responsible for the food efficiency of the diet. Consequently, the carbohydrate content of the diet is correlated directly with weight gain and adiposity. Second, carbohydrate is the main secretagogue of insulin, which stimulates fat storage. If lipid is associated with a high carbohydrate content, which is the case for the P14C76L10 diet, it leads to the development of adiposity. On the contrary, in the absence of carbohydrate in the diet (P55L45 group), insulinemia remains low, and lipid oxidation is increased at the expense of lipid deposition. Consequently, the lowest C:L ratio (C:L = 0), induced the lowest weight gain, fat body mass, adipocyte size, total adipocyte number, and fatty acid synthase activity. These results agree with those of Klein and Wolfe (16), indicating that the carbohydrate level of the diet appears to be the most important factor in driving lipid metabolism. Third, the reduction in liver FAS produced by reducing the C:L ratio was in line with previous observations (17,18). Indeed, genes coding for fatty acid synthesis enzymes are activated in response to a high carbohydrate content in the diet (19,20). In rats fed the control diet with a high carbohydrate content, some of the glucose-derived acetyl CoA was used as a precursor for fatty acid synthesis. Decreasing the carbohydrate content in the diet led to a reduction in FAS expression and activity, and in the flux of glucose to fatty acid synthesis, which subsequently reduced adipocyte size and fat mass.

In contrast, the precise origin of the reduction in the number of adipocytes, which was specific to the P55L45 diet and was not observed with the P55C35L10 diet, remains to be determined. It likely originated in part from the more efficient downregulation of FAS and fatty acid synthesis in the liver, inducing a decrease in fatty acid availability in adipose tissue that ultimately reduced adipocyte differentiation. Other specific effects of amino acids and fatty acids on adipose tissue differentiation may also be involved.

In conclusion, the present study confirms the appetite suppressive effect of protein and reinforces the idea of the crucial role of the carbohydrate:fat ratio in the control of lipid metabolism. As observed previously, increasing the amount of protein in the diet, in the context of a low or high fat content, decreased energy intake more than a high-carbohydrate, normal-protein diet. In addition, a high-protein, high-fat, carbohydrate-free diet did not further modify energy intake. As a consequence, the reduction in food intake is a specific effect of protein. This study also demonstrated the major role of the carbohydrate:lipid ratio of the diet. First, glucose is the main secretagogue of insulin, and consequently stimulates energy storage, particularly fat storage. Furthermore, carbohydrates activate genes coding for FAS, which also contribute to fat storage. Finally, lowering the carbohydrate content of the diet enhances gluconeogenic activity and consequently reduces energy storage as fat storage because of the high energetic cost of gluconeogenesis. Extrapolation of these results to humans requires additional study because de novo lipogenesis is thought to be less marked in humans than in rats. Nevertheless, it seems that high-fat, carbohydrate-free diets are able to enhance nutritional status by reducing fatty acid de novo synthesis and fat storage. Moreover, these diets, although unusual, meet nutritional requirements because dietary carbohydrates are not indispensable and their absence can be compensated by gluconeogenesis.


   FOOTNOTES
 
2 Abbreviations used: AI, adiposity index; BSA, bovine serum albumin; C:L, carbohydrate:lipid; FAS, fatty acid synthase; LPL, lipoprotein lipase; P14C76L10, diet containing 14% protein, 76% carbohydrate, and 10% fat; P55C35L10, diet containing 55% protein, 35% carbohydrate, and 10% fat; P55L45, diet containing 45% as fat and 55% as protein; SBAT, scapular brown adipose tissue; WAT, white adipose tissue. Back

Manuscript received 14 November 2005. Initial review completed 23 November 2005. Revision accepted 6 January 2006.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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