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Lipid analysis of tissues from camel (Camelus

dromedaries) reveals unique composition in fatty acids

Boubker NASSER(1)*, M’hamed Said EL KEBBAJ(2), Khadija MOUSTAID(1), Abdallah BAGRI(1), Abdelkhalid ESSAMADI(1) and

Norbert LATRUFFE(3)

Abstract— Domesticated Arabian camel, Camelus dromedarius, is the most important animal in arid and semiarid areas, as it represents the main source of meat, milk and fat besides its high cultural and economical values. The present work was carried out to determine the compositions of fatty acids and phospholipids in the hump, plasma and liver mitochondria were studied under various physiological and nutritional conditions of this ruminant. In plasma, palmitic (C16:00), linoleic (C18:2 n-6), stearic (C18:00) and oleic (C18:1 n-9) acids represent 70% of the fatty acids identified. In liver mitochondria, a closely similar ratio was obtained (62%) but with different proportions. In the hump, palmitic, oleic, stearic and myristic acids represent 82% of the total fatty acids. Moreover, qualitative differences were observed with myristic (C14:00) acid whereas linoleic acid was lacking. The phosphatidylcholine and phosphatidylethanolamine are the major mitochondrial phospholipids with (62%) whereas sphingomyelin represent (14%), while phosphatidylinositol shows the weakest rate (5%). The composition of fatty acids (chain length and unsaturation) in plasma and in liver mitochondria did not depend on age, sex, mass and diet. These results shows qualitative similarity in the composition of fatty acids between plasma and liver mitochondrial membranes but not with in the hump. These results suggest that the camel developed a particular metabolic regulatory system to maintain constant the composition of fatty acids independently of physiological and the nutritional conditions.

Index Terms— Camel, plasma, mitochondria, hump, membrane, fatty acids, phospholipids.

——————————  ——————————

1 INTRODUCTION

HE camel (Camelus dromedaries; one-humped camel) be- longs to the family Camelidae, genus Camelus. It has been domesticated for about 4000 years and has been long val-
ued as a pack animal. The camel is a domesticated ruminant species of considerable biological and economic importance, especially in arid and semi-arid regions [1], [2]. To survive in these difficult conditions and thanks to these anatomical and physiological characteristics, the camel has adapted by mech- anisms of resistance to protein under nutrition (urea recy- cling), energy (fat reserves of the hump), water (resistance to thirst), but also mineral [3], [4], [5], [6], [7], [8], [9], [10].
In the north of Africa, Middle East and Asia, camels play a critical role in providing human foods, especially meat, milk and fat [11], [12], [13], [14], [15]. Camel fats, are used to pre- pare many dishes, namely, the production of a cocoa-butter analog [11], [16], making high-quality dry sausages, and frying [17], [18], [19]. The body lipids are the main form energy stor- age in mammals. Lipid deposition and mobilization cycles are essential for reproduction, lactation and ecological adaptations [20]. The adipose reserves in camels are mainly stored in the hump [21], [22], [23], [24]. However, changes in lipid reserves and related mechanisms are not well understood in this spe- cies which is able to survive long periods without feed [9],

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(1) Laboratory of Biochemistry and Neuroscience-Team Biochemistry and Toxicology Applied, University Hassan First - Faculty of Sciences and Techniques, BP 577, Settat, Morocco

(2) Laboratory of Biochemistry, Faculty of Sciences Ben M’Sik, Casablanca,

Morocco

(3) Laboratory of Biochemistry (BioperoxIL), University of Bourgogne,

LBMN, 6, Bd Gabriel, 21000 Dijon, France

* Corresponding author. Fax: +212523402612; E-mail:

boubker_nasser@hotmail.com

[25]. Despite these difficult survival conditions, the trans-fatty acid profile of lipids from hump adipose tissue and milk was compared in camel and cattle, and shows that there are no gross differences between the two species [26]. Moreover, D-3- hydroxybutyrate dehydrogenase, a mitochondrial inner mem- brane bound enzyme was discovered and purified an unique structure in camel and involved in the conversion of ketone bodies as products of lipid metabolism [27]. Additionally, most of fatty acids in the camels are esterified as triglycerides or phospholipids and vary according to their anatomical loca- tion in the body [28], [29]. All these literature results suggest the existence of a very developed system of regulation in the dromedary which is determined probably by the environment.
Data on the composition of camel fats are relatively scarce and few available in the literature. In fact, most studies on li- pid composition in camels have been reported especially in milk [30], [31], [32] and meat [33], [34], [35]. To our knowledge, no analytical work has so far been undertaken on lipid con- tents in camel tissues in Morocco. The present study was aimed at investigating the fatty acids and phospholipids com- position in the hump, plasma and liver mitochondria under various physiological and nutritional conditions of this ani- mal.

2 MATERIALS AND METHODS

2.1 Materials

A group of 20 camels, 13 females and 7 males, aged 7 to 14 years old and weighting between 333 to 470 kg, raised at the Bouskoura experimental station of the National Institute for Agronomic and Veterinary Sciences Hassan II (Casablanca) (see Table 1) under controlled conditions, or overfed. Blood

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samples were taken at the jugular vein and were immediately
centrifuged and the supernatant was frozen at -28ºC until analysis.
The samples of liver and hump from 3 females and 3 males (age: from 6 months to 3 years) were collected accompanied by a veterinary hygiene inspector, after sacrificing the animals at the slaughterhouse. The livers where immediately placed in a sucrose cold solution 0.25 M pH 7, used for the preparation of homogenate and mitochondria.

2.2 Methods

2.2.1 Mitochondrial isolation and separation of the membranes

The preparation of the mitochondria was done according to the adapted method of Fleischer et al., [36]. The liver samples were immediately washed and crushed in a solution of su- crose 0.25 M pH 7 with the Ultra turrax (for 2 seconds at low speed), pottered then filtered on layers of pharmaceutical gauze then centrifuged. The mitochondria thus obtained were suspended in a minimum of Hepes buffer 10 mM pH 7.4 con- taining sucrose 0.25 M then frozen in nitrogen atmosphere and stored at -28ºC until use. An aliquot was taken, protein con- centration was determined as described by Lowry et al., [37] and phosphorus concentration was determined as described by Chen et al., [38]. The mitochondrial membranes were iso- lated according to the method of Kielley and Bronk, [39]. Fro- zen samples of mitochondria were thawed in buffer phosphate
20 mM pH 7.4, at a ratio of 0.5 ml of buffer per mg of protein. After centrifugation at 20 000 g for 10 min at 4ºC, the pellet contains the inner membranes while, the supernatant contains the outer membranes and the content of the intermembranar space. The various fractions obtained were frozen in nitrogen atmosphere and stored at -28ºC until use.

2.2.2. Extraction of phospholipids

After thawing the samples of plasma, hump and mitochondri- al membranes, the extraction of lipids was carried out accord- ing to the method of Folch et al., [40]. The sample was crushed with the Ultra turrax, in 20 volumes of the chloro- form/methanol 2/1 (v/v) mixture. The lipid extract was washed with KCl aqueous 0.2 volume by volume of a 0.8% (w/v) solution. The organic phase was then recovered and washed with the chloroform/methanol/potassium chloride mixture 0.8% (w/v) in proportions 3/48/47 (v/v/v). The chloroform phase was filtered and then evaporated with a rotary evaporator. The residue obtained, made up of total li- pids, was dissolved in a minimum of extraction solvent then stored at -28°C, under nitrogen until use.

2.2.3. Preparation of fatty acids methyl esters

The transformation of the fatty acids of phospholipid esters to methyl esters was carried out according to the method of Morisson and Smith, [41]. It consisted of a transmethylation of lipids by methanol catalyzed by boron trifluoride (12% in methanol), then heated at 100°C for 60 min. According to the type of lipids. The methyl esters of the lipid phase were ex- tracted with hexane and washed with distilled water. To sepa- rate the saturated fatty acids from the unsaturated acids ac-

TABLE 1

PHYSIOLOGICAL (AGE, MASS) AND NUTRITIONAL (*FU/D: FORAG- ER UNIT/DAY) CONDITION OF CAMELS IN THE EXPERIMENTAL STA-

TION

The food composition was barley, hay and industrial food (from Alf Sahel, Had

Soualem Morocco).

cording to the method of Folch et al., [40], the solvent was evaporated and total fatty acids methyl ester were submitted to fractionation by thin-layer chromatography on a silica plate impregnated with silver nitrate.

2.2.4. Separation of phospholipids

The thin-layer chromatography was carried out on Silicagel
60. After depositing the sample on the chromatography plate,
a first migration was carried out in a mixture of chloro-
form/methanol/water 65/25/4 (v/v/v) for separation of four
spots which were revealed with the 2,7-dichlorofluorescein.
The three spots of weak follow reference were scraped off and
the phospholipids were extracted using the mixture chloro-
form/methanol 2/1 (v/v). The extracts thus obtained were
deposited separately on another plate. A second migration was then carried out, according to the method of Heape et al., [42], in 0.25% chloride potassium mix- ture/methanol/propane/methyl acetate/chloroform
3/2.7/8.6/10/8.6 (v/v/v/v/v). After identification with the
2,7-dichlorofluorescein, each phospholipid class was collected
in order to prepare methyl esters as described previously, to
be analyzed by gas chromatography.

2.2.5. Identification and quantitative estimation of fatty acids

The identification and quantification of fatty acids methyl es- ters derivatives previously prepared was carried out on a Car- lo Erba HRGC 5300 chromatograph equipped with a flame ionization detector connected to an integrator Spectra-physics SP 4290. The capillary column was a DB Wax, (J & W Scien- tific, Folsom, CA) with a length of 30 m and an inner diameter of 0.32 mm, with a film thickness of 0.5 mm. The separation was carried out under isothermal conditions at 190°C. The temperature of the injector and of the detector was 250°C. The carrier gas was helium at a pressure of 140 kPa.

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3 RESULTS AND DISCUSSION

3.1 Fatty acids composition of plasmatic phospholipids The analysis of the fatty acid composition in plasmatic phos- pholipids of the camel showed that palmitic (25.61±3.2%),

stearic (16.47±2.13%), oleic (16.88±2.40%) and linoleic
(16.62±2.05%) acids, represent more than 70% of total fatty
acids. Arachidonic (C 20:4 (n-6)) acid did not exceed
3.61±1.01%. The other fatty acids were present as traces (Table
2).

TABLE 2

PLASMATIC, LIVER MITOCHONDRIAL AND HUMP FATTY ACIDS COM- POSITION (IN PERCENT OF TOTAL LIPIDS)

The comparative study of the composition of plasmatic fat- ty acids did not show any significant difference between the effect of various physiological (sex, age, weight) and nutri- tional (food intake) conditions of the camel (Table 1). The ratio of saturated to unsaturated fatty acid was not affected (0.86). The comparison between these results and those already ob- tained in the rat shows that the phospholipids fatty acid com- position and unsaturated/saturated ratio change with age and diet [43], [44], [45], as well as for beef [46]. In spite of our re- sults concerning the fatty acid composition in plasmatic phos- pholipids of the camel, a recent study reported that only four fatty acids were widely present in the serum of camel. Palmitic acid, stearic acid, oleic acid and linoleic acid representing 89.1 of the whole fatty acids [30]. On the other hand, fatty acid pro- files in erythrocyte lipid composition in sheep showed five main acids: oleic, stearic, linoleic, palmitic and arachidonic acid [47].

3.2 Fatty acids composition of total mitochondrial phospholipids

The analyses of fatty acids composition of total phospholipids of the camel liver mitochondrial membranes are presented on Table 2. Palmitic, stearic, oleic and linoleic acids are the most abundant, with more than 63% of total fatty acids, with per- centages of 18.24±3.52%; 22.67±2.93%; 8.12±1.05% and
13.25±2.32% respectively. Arachidonic acid represents
7.87±1.40%.
The effect of age, sex and nutrition of the camel (Table 1) on
the composition of total mitochondrial fatty acids is not signif-
icant. The comparison between the results obtained in this
study and those described in the rat by Stoffel and Schiefer,
[48] shows that the composition of these fatty acids in the mi-
tochondrial membranes of the rat represents more than 76%.
Indeed, the palmitic and stearic acids account for 49% of total
fatty acids of the mitochondrial membranes of the rat. On the other hand, in the camel these same fatty acids only account for 39%. Arachidonic acid accounts for only 7.87±1.40% in the camel whereas in the rat, it represents more than 19.5%. This
low amount of arachidonic acid may be explained by the low gamma-linolenic C18:3 n-3 acid content in the mitochondria or its total absence in the plasma since the gamma-linolenic acid is the first precursor in the enzyme conversion limiting step of linoleate into arachidonate [49]. The possible low activity of the delta-6-desaturase (E.C.1.14.99.5), the enzyme responsible for conversion of 6-linoleic acid into gamma-linolenic acid [50], [51] could also give another reason. Moreover, this meta- bolic process, seems to be highly affected by certain physiolog- ical processes such as the feeding [52], the hormonal statute or the age of the animal in the rat [53], the weight and nutrition

For plasma the data represent the mean on 13 animals (see Table 1), for liver mitochondria and hump the data correspond to the mean 6 slaughtered animals (see materiel and methods paragraph 2.1.). *Ratio: saturated fatty ac- ids/unsaturated fatty acids.

in the beef [46]. This phenomenon was not seen in the camel. In spite of our results, Shibani et al., [54] reported that in camel liver, the most abundant fatty acids were oleic acid, palmitic acid and stearic acid. In the liver, relatively high levels of lino- leic acid were found which is attributable to their higher per- centage of phospholipids in total lipids than in the other tis- sues where triglycerides are the predominant lipids [54].

3.3 Fatty acids composition of hump phospholipids

The analysis of fatty acids composition in the hump showed that the myristic (8.93±1.43%), palmitic (37.2±2.65%), stearic (14.8±2.16%) and oleic (19.61±1.28%) acids represent the ma- jority of the fatty acids (Table 2). These fatty acids constituted more than 82%. The other fatty acids were present as traces.
Our results were comparable with those reported in a re- cent study concerning the fatty acid composition from the hump of young camels (Hachi), where the most important acids were oleic, palmitic, stearic, palmitelaidic and myristic acid, which together accounted for approximately 88% of the total fatty acids [55]. Similarly, Shibani et al., [54] have showed that the most abundant fatty acids in lipids from camel hump were oleic acid, palmitic acid, stearic acid and myristic acid. A study performed by Kadim et al., [24] on concentrations of fatty acids in the hump and abdomen fats of three different age groups of camel reported that palmitic acid was the major fatty acid in hump fat, followed by oleic acid and stearic acid. Kadim et al., [24] have also mounted that the young camels have less total fatty acids than older camels in the hump.

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However, age has little effect on fatty acid composition. Thus,
our results are in agreement with the findings reported in the literature [29], [56], [57], [58], [59].
However, concerning ketones bodies level, other report [60], [61] shown differences which are in accordance with the dependency of ketonic bodies concentration to the regional breeding (unpublished work), The determination of the ratio of saturated to unsaturated fatty acids Table 2, showed that this ratio is about twice higher in the hump than in the mito- chondria. This ratio is 0.84% in the mitochondria and 1.92% in the hump.

3.4 Fatty acids composition of mitochondrial phospholipids

Analysis of the results, represented in Table 3, showed that PE and PC constituted the major fraction of total liver mitochon- drial phospholipids, with percentages of 31.6% and 30.6% re- spectively. The class of PI had weakest fraction with 5.1%.
The same qualitative composition was obtained by Stoffel and Schiefer, [48] in the rat where PC and PE account for 41% and 35% respectively of total mitochondrial phospholipids. PI accounts for only 2%. However, the SM fraction which repre- sented 14% of total phospholipids in the camel seems occur only as traces in the rat and in bovine as described by Fleischer et al., [62] and by Stoffel and Schiefer, [48].
The distribution of the fatty acids in the various phospho- lipid classes shows that linoleic acid is the major component in PC and PS, with 12.3%, followed by stearic acid, with 11.5%. In PE and PI, the stearic acid accounts for 28.6 and 32% respec- tively. For the CL the linoleic acid represents more than one- half of the total fatty acids with 52%. Whereas, for SM the palmitic acid is the major fatty acid with 13.8%, followed by stearic acid with 12.1%. The comparison between the results obtained here and those already obtained by Stoffel and Schiefer, [48] in the rat, shows a quantitative and qualitative difference in the levels of the fatty acids and of the various classes of phospholipids and especially at the level of the ara- chidonic acid and SM.
The analysis of the composition of fatty acids from inner
membrane lipids (Table 3) of the camel liver mitochondria
shows that, in PC, PE and PI, the stearic acid is the major fatty
acid with 28.8%, 40.7% and 51.4% respectively, followed by
palmitic acid with 20.1%, 12.4% and 14% respectively. For the
CL the linoleic (C18:2 (n-6)) acid represents more than 44%.
For SM, palmitic acid is the major fatty acid with more than
33% followed by oleic acid 25.5%. The study of the composi-
tion in fatty acids of the inner membrane compared to the
whole mitochondria shows a clear predominance of stearic
acid in PC, PS, PE. But for PI, CL and SM qualitative and
quantitative difference were observed for the composition of phospholipid fatty acids.
Table 2 shows the ratios of saturated/unsaturated fatty ac- ids change, it was 0.88, 0.85 and 1.74 respectively in plasma, in mitochondrial phospholipids and in hump. The distribution of this ratio in the different classes of mitochondrial phospholip- ids. The composition of total fatty acids in the hump was char- acterized by a high rate of saturated fatty acids: Myristic, pal- mitic and stearic represent the majority of total fatty acids. In the other hand, the ratio of saturated to unsaturated fatty acids

TABLE 3

COMPARED FATTY ACIDS COMPOSITION OF PHOSPHOLIPIDS IN LIVER MITOCHONDRIA AND IN INNER MITOCHONDRIAL MEMBRANE

FROM CAMEL

is similar in plasma and in mitochondria. The difference ob- served in the hump explain by the higher level of saturated fatty acids.
In mitochondria, the distribution of this ratio was function of the different class of phospholipids studied. According to our results, we distribute the ratio of different phospholipids in three groups: The first group of PI that represents the high- est ratio the stearic and palmitic acids are major in this compo- sition. The second group of PC, PE, PS and SM that represent the means ratio being given the equivalence in saturated and unsaturated fatty acids and the third group of CL that repre- sents a weak rate. In comparison with the results found in the rat, as already described [48], the analysis of the results ob- tained with camel reveal that these ratios are higher in the rat. Therefore, the rate of unsaturation is higher in the camel than in the rat. Only the cardiolipins showed a higher ratio. This could be explained by the low amount of linoleic acid in the camel compared to the rat.
Warda and Zeisig, [63] reported that the most frequently occurring lipids of the membrane of erythrocytes from the one-humped camel are sphingomyelin, phosphatidylcholine and phosphatidylserine. On the other hand, our results of total liver mitochondrial phospholipids in camel were in the range reported in the literature for cattle milk: PE (19.8-42.0%, w/w), PC (19.2-37.3%, w/w), PS (1.9-10.5%, w/w), PI (0.6-11.8%, w/w) and SM (18.0-34.1%, w/w) [64], [65], [66], [67], [68].
On the other hand, in camel meat, the major fatty acids are palmitic, oleic and linoleic, with smaller amounts of other fatty acids, both normal and branched [33], [34], [59], [69]. Kadim et al., [70] indicates that the fat content of camel meat may in- crease with age. For against, the comparison by age showed no significant effect on the content of fatty acids [35]. Also, the main milk fatty acids in camel milk were myristic acid, palmit- ic acid, palmitoleic acid, stearic acid and oleic acid represent- ing as the whole 86.7% of the milk fatty acids [30]. The varia- tion in fatty acids concentrations in milk could be due to dif- ferences in the type of feed, breed and stage of lactation

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amongst animals [31]. Palmquist et al., [71] reviewed other factors, which affect fatty acid composition like animal genet- ic, grain, amount and composition of dietary fat, dietary pro- tein, seasonal and regional effects.

4 CONCLUSION

The study of the qualitative and quantitative composition of phospholipids and fatty acids of the camel showed that pal- mitic, stearic and oleic and linoleic acids, are the major fatty acids of plasma and liver mitochondrial inner and outer mem- branes with equivalent proportions, in contrast to another species, the rat. The composition of fatty acids in the hump was characterized by higher level of saturated of fatty acids with a majority of myristic, palmitic and stearic acids. Plasma and liver mitochondrial membranes of camel are characterized by a low level of arachidonic acid. This low content may be due to the low levels of it precursors or to the low expression of the arachidonic acid biosynthesis enzymes. The comparison of the ratios between saturated and unsaturated fatty acids shows that the camel is characterized by membranes much less rigid than the rat.

ACKNOWLEDGMENT

This work was supported in part by CNRST-Maroc pro- gramme recherche sectorielle (RS/26) Morocco.

ABBREVIATIONS

Mito: mitochondria; IMM: inner mitochondrial membrane; PC: phosphatidylcholine; PE: phosphatidylethanolamine; SM: sphingomyelin; PI: phosphatidylinositol; PS: phosphatidylser- ine; CL: cardioloipines; SFA: saturated fatty acids; UFA: un- saturated fatty acids.

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