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Stearoyl-Coenzyme A Desaturase Gene Polymorphism and Milk Fatty Acid Composition in Italian Holsteins

M. Mele^*,1, G. Conte^*, B. Castiglioni, S. Chessa, N. P. P. Macciotta, A. Serra^*, A. Buccioni^#, G. Pagnacco and P. Secchiari^*

^* Dipartimento di Agronomia e Gestione dell’Agroecosistema, University of Pisa, Italy
Istituto di Biologia e Biotecnologia Agraria, CNR, Milan, Italy
Dipartimento di Scienze e Tecnologie Veterinarie per la Sicurezza Alimentare—University of Milan, Italy
Dipartimento di Scienze Zootecniche, University of Sassari, Sassari, Italy
^# Dipartimento di Scienze Zootecniche, University of Florence, Florence, Italy

¹ Corresponding author: mmele{at}agr.unipi.it

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Milk fatty acid composition is a parameter of great interest for evaluation of nutritional quality of milk. Stearoyl-CoA desaturase (SCD) is a key enzyme in mammary lipid metabolism because it is able to add a double bond in the cis ⁹-position in a large spectrum of medium- and long-chain fatty acids. A polymorphism with 2 alleles (A and V) in the fifth exon of the SCD gene has been reported. The effect of SCD genotype on individual milk fatty acid composition and on cis-9 unsaturated/saturated fatty acid ratios of 297 Holstein Italian Friesian cows was investigated in this paper. The SCD genotypes were determined by using a single strand conformation polymorphism method. Relative frequencies of SCD genotypes were 27, 60, and 13% for AA, AV, and VV, respectively. Milk of AA cows had a greater content of cis-9 C18:1 and total monounsaturated fatty acids and a higher C14:1/C14 ratio than did milk of VV cows. The relative contribution of SCD genotype to variation of monounsaturated fatty acids, cis-9 C18:1, and cis-9 C14:1 was 5, 4, and 7.7%, respectively. No significant differences were detected between SCD genotypes in the milk content of cis-9, trans-11 C18:2. Results of the present work provide some indication of an association between SCD locus and the fatty acid profile in the examined sample of Italian Holsteins, thus suggesting a possible role of this gene in the genetic variation of milk nutritional properties.

Key Words: stearoyl-CoA desaturase polymorphism • conjugated linoleic acid • monounsaturated fatty acid

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
The fatty acid (FA) fraction of ruminant’s milk contains several compounds of great interest for human health, such as monounsaturated FA (mainly oleic acid) and conjugated linoleic acids (CLA). Studies aimed at finding efficient strategies to improve the nutritional quality of milk concluded that feeding supplementation is the most efficient way to modify milk FA (Palmquist et al., 1993; Jenkins and McGuire, 2006), even if a recent study suggested that the genetic improvement of the nutritional quality of milk based on FA profile may be possible (Soyeurt et al., 2006). However, traditional selection programs based on performance recording and prediction of breeding values could be constrained by the high costs for the measurement of phenotypes. The search for loci affecting FA profiles and their use in marker assisted selection programs offer an alternative to modify nutritional qualities of milk through genetic selection.

Among the several enzymes known to affect the lipid metabolism of the mammary gland, the stearoyl-CoA desaturase enzyme (SCD; also known as ⁹-desaturase) plays a key role because it introduces a double bond at the ⁹-position in a large spectrum of FA (Ntambi, 1999; Ntambi and Miyazaki, 2004). Its most important substrates are acyl-CoA of C14, C16, C18, and trans-11 C18:1 (known as vaccenic acid), which are converted into C14:1 n-5, C16:1 n-7, cis-9 C18:1, and cis-9, trans-11 C18:2, respectively (Corl et al., 2001), the latter being a CLA isomer of great interest due to its antiatherogenic, anticarcinogenic, and immunomodulating properties (Pariza, 1999). More than 70% of the cis-9, trans-11 CLA of ruminant’s milk is produced in the mammary tissue by the activity of SCD (Bauman et al., 2006).

The SCD locus has been mapped on the bovine chromosome 26. It is 17,088 bp long with an open reading frame of 1,080 bp and codes for 359 amino acids. Three single nucleotide polymorphisms (SNP) in complete linkage disequilibrium and that result in 2 haplotypes have been detected in the fifth exon (Taniguchi et al., 2004). The third SNP causes the substitution of valine (allele V) with alanine (allele A) on the 293rd residue (Figure 1). Because valine is highly conserved across mammals, it is considered the ancestral amino acid in that position (Taniguchi et al., 2004). The SCD polymorphism has been found in Holstein Friesian, Jersey, Brown Swiss, and Japanese Black cattle breeds (Medrano et al., 1999; Taniguchi et al., 2004).

View larger version (12K): [in this window] [in a new window]   Figure 1. Bovine stearoyl-CoA desaturase (SCD) polymorphism. The gray boxes show the nucleotide substitution that causes the amino acid replacement valine 293alanine 293.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Animals
The analysis was carried out on 297 Italian Holstein Friesian cows sampled from 21 half-sib families (14 ± 2 daughters per bull) and distributed in 34 herds (9 ± 3 cows per herd) located in the northeast of Italy.

DNA Extraction and Amplification
Genomic DNA was extracted from milk somatic cells with the GFX Genomic Blood DNA Purification Kit (Amersham Biosciences, Uppsala, Sweden) following the supplier’s protocol with some modifications. Briefly, 900 µL of RBC lysis solution were added to 300 µL of milk in a 1.5-mL microcentrifuge tube, incubated at room temperature, and then centrifuged at 11,300 x g for 1 min. The supernatant was removed, and the residual fluid was vortexed and then mixed with 500 µL of extraction solution and incubated at room temperature. The mixture was then transferred to the GFX column and centrifuged at 4,300 x g for 2 min. The DNA was removed with an extraction solution (buffered solution containing chaotrope and detergent) and centrifuged again at 4,300 x g for 2 min. A second washing with 500 µL of wash solution (Tris-EDTA buffer added with absolute ethanol) was performed, followed by a full speed centrifuge (11,300 x g) for 4 min. The GFX column was transferred into a fresh 1.5-mL tube for the elution. One hundred microliters of 70°C preheated double-distilled water were added directly to the fiberglass matrix of the column. After 1 min of incubation at room temperature, the tube was centrifuged at 4,300 x g for 2 min to collect the purified DNA.

The fifth exon region of the SCD gene was amplified by PCR (GeneAmp PCR 9600; Perkin Elmer Life Sciences). Specific primers were designed on the basis of the bovine SCD gene sequence (Medrano et al., 2003, accession no. AY241932) at GenBank (Figure 2):

View larger version (32K): [in this window] [in a new window]   Figure 2. Positions of stearoyl-CoA desaturase (SCD) primers. Bold type shows the SCD gene fifth exon. The primers were designed by Medrano et al. (2003).

SCD-9848F: 5'-CAGTCCTTGCTCCACCACTT-3';

SCD-10572R: 5'-AGCATTTGTGGCTTGCTCTT-3';

SCD-9961F: 5'-CCCATTCGCTCTTGTTCTGT-3';

SCD-10355R: 5'-GTCTTGCTGTGGACTGCTGA-3'.

The DNA was preheated at 94°C for 5 min and then amplified with 30 cycles of 94°C for 45 s, 56°C for 45 s, and 72°C for 1 min. The final cycle had an extension time of 7 min at 72°C. The PCR reaction was performed using a mix of 12.5 µL of 2x PCR Master Mix (Fermentas International Inc., Burlington, Canada; Taq DNA polymerase 0.05 units/µL, MgCl₂, 4 mM, and dNTP, 0.4 mM of each), 0.5 µL of 10 pmol/µL primer forward, 0.5 µL of 10 pmol/µL reverse primer, 250 ng of DNA and ddH₂O up to 25 µL. Among the several PCR products, the 725-bp fragment obtained using SCD-9848F and SCD-10572R primers was retained for the genotyping (Figure 3).

View larger version (38K): [in this window] [in a new window]   Figure 3. The PCR products: lane 1 and 6- GeneRuler 1 kb DNA ladder (Fermentas International Inc., Burlington, Canada); lane 2-SCD-9848F/SCD-10355R product (508 bp); lane 3 SCD-9848F/SCD-10572R product (725 bp); lane 4 SCD-9961F/SCD-10572R product (612 bp); lane 5 SCD-9961F/SCD-10355R product (395 bp).

DNA Sequencing
The DNA samples with different SSCP gel patterns were further sequenced by PRIMM Srl (Milan, Italy). One sample for every assumed genotype was randomly chosen. Primers used for sequencing were the same of the PCR-SSCP analysis. Nucleotide sequences were analyzed with Chromas 2.24 software (Technelysium Pty Ltd.).

Milk Fat Analysis
Individual milk samples were taken at the morning milking and stored at –20°C. One milk sample was taken per animal. Milk fat was extracted following the Rose-Gottlieb method (AOAC, 1990) modified by Secchiari et al. (2003). Two grams of milk were mixed with 0.4 mL of ammonia 25%, 1 mL of ethyl alcohol 95%, and 5 mL of hexane, vortexed, and centrifuged at 1,600 x g and 4°C. The upper layer was collected, and a second extraction with 1 mL of ethyl alcohol 95% and 5 mL of hexane was performed. A third extraction was made using 5 mL of hexane. The extracted fat was dried, weighed, and finally dissolved in hexane. Methyl esters of medium- and long-chain fatty acids were prepared by Christie’s alkali catalyzed transmethylation procedure (1982) with nonadecanoic acid methyl ester (Sigma Chemical Co., St. Louis, MO) as the internal standard. Medium- and long-chain FA composition was determined by gas chromatography using a ThermoQuest (Milan, Italy) gas-chromatograph equipped with an FID and a high polar fused silica capillary column (Chrom-pack CP-Sil 88 Varian, Middelburg, the Netherlands; 100 m x 0.25 mm i.d.; film thickness 0.20 µm). Helium was used as the carrier gas at a flow of 1 mL/min. The split ratio was 1:100. An aliquot of the sample was injected under the following GC conditions: the oven temperature was programmed at 120°C and held for 1 min, then increased to 180°C at a rate of 5°C/min, held for 18 min, increased to 200°C at 2°C/min, held for 1 min, increased to 230°C at a rate of 2°C/min and held for 19 min. The injector temperature was set at 270°C, whereas the detector temperature was set at 300°C. Cis and trans C18:1 isomers were determined on a second aliquot of the same sample at 175°C (isothermal step) for 65 min using the same capillary column. Individual FA methyl esters were identified by comparing them to a standard mixture of 37 Component FAME Mix (Supelco, Bellefonte, PA). The standards PUFA-2, non-conjugated C18:2 isomer mixture, individuals cis-5,8,11,14,17 C20:5, cis-4,7,10,13,16,19 C22:6 (Supelco), cis-6,9,12 C18:3 and cis-9,12,15 C18:3 (Matreya Inc., Pleasant Gap, PA) were used to identify polyunsaturated FA. The identification of C18:1 isomers was based on commercial standard mixtures (Supelco) and published isomeric profiles (Wolff and Bayard, 1995). All the methods that use peak normalization and that express results as a relative percentage of the area of the analyzed peaks are subject to overestimation because of small peak areas not considered. To avoid this problem, a nonadecanoic acid as internal standard was used and all milk FA compositions were expressed as g/100 g of fat.

Ratios of Milk Fatty Acids
The extent of FA desaturation was determined by calculating the ratio of cis-9 unsaturated to cis-9 unsaturated + saturated for specific FA (Sol-Morales et al., 2000; Palmquist et al., 2004). The following ratios were calculated: cis-9 C14:1 to cis-9 C14:1 + C14:0 (C14:1/ C14); cis-9 C16:1 to cis-9 C16:1 + C16:0 (C16:1/C16); cis-9 C18:1 to cis-9 C18:1 + C18:0 (C18:1/C18); cis-9, trans-11 CLA to cis-9, trans-11 CLA + trans-11 C18:1 (CLA/trans-11 C18:1).

Moreover, a general index of desaturation (DI) was calculated (adapted from Malau-Aduli et al., 1997):

Statistical Analysis
Data were analyzed with the following mixed linear model (SAS, 1999):

[1]

where y_jklmno = dependent variable (milk fatty acids as g/100 g of lipids, and FA ratios); µ = overall mean; HERD _j = fixed effect of the jth herd (34); PARITY_k = fixed effect of the kth parity (first, second, third); DIM_l = fixed effect of the lth days in milking interval (<100, 100 to 200, >200); SEASON_m = fixed effect of the mth calving season (winter, spring, summer, autumn); SCD _n = fixed effect of the nth SCD genotype (AA, AV, VV); SIRE_o = random effect of the oth sire (21); and _jklmno = random residual. Results on the SCD genotype effects were presented as least square means ± SE, and linear contrasts were tested between AA and AV genotypes and between AV and VV genotypes.

The average gene substitution effect for the SCD locus on milk FA content was calculated according to Falconer and McKay (1996). The contribution of the SCD locus to the variability of the traits considered was assessed by calculating the reduction of residual variance observed in the full model [1], in comparison with a reduced model that did not include the SCD genotype as fixed factor (Neter et al., 1996).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Three different patterns were detected by the PCR-SSCP analysis of the DNA fragment containing the polymorphism of the SCD gene (Figure 4). The occurrence of a single lower or upper band was considered as evidence for a homozygous AA or VV, respectively, whereas both bands were regarded as an evidence for a heterozygous AV. This genotype assignment was confirmed by nucleotide sequencing. The different SSCP patterns corresponded to the third SNP (Figure 5): alleles V and A match the upper and the lower band, respectively.

View larger version (24K): [in this window] [in a new window]   Figure 4. The PCR-single strand conformation polymorphism (SSCP) analysis for the fifth exon of the stearoyl-CoA desaturase (SCD) gene polymorphism. The white and the black dots indicate the occurrence of A and V, respectively.

View larger version (25K): [in this window] [in a new window]   Figure 5. Nucleotide sequence results. The figure shows a region around the third single nucleotide polymorphism of a heterozygous sample, which is indicated by the 2 arrows.

The relationship between SCD polymorphism and milk cis-9, trans-11 CLA content is of particular interest. Milk cis-9, trans-11 CLA content is characterized by individual variation (up to 8-fold) that can be observed in cows fed the same diet (Bauman et al., 2001; Chilliard et al., 2001; White et al., 2001; Secchiari et al., 2003). Therefore, an important role of the genetic background of animals could be hypothesized. In our study, the AA genotype was associated with 12% more cis-9, trans-11 CLA when compared with VV; however, this difference did not reach the level of significance (P = 0.19), perhaps due to the small size of the sampled population.

In terms of explained variance, the contribution of SCD genotype to MUFA variation in milk fat was quite low (5%), in agreement with results reported for intramuscular fat in cattle (Taniguchi et al., 2004). Of the same magnitude are contributions of the SCD genotype to cis-9 C18:1, and cis-9 C14:1 variation (4 and 7.7%, respectively). These results suggest a reproducible and ubiquitous effect of the amino acid substitution. The contribution of SCD genotype to the total variation of other FA profiles was nonsignificant and less than 1%.

Sire effects accounted for 6, 5, and 8% of the total variance for content of cis-9 C18:1, and cis-9 C14:1, and MUFA, respectively. These values are indicative of an appreciable additive genetic effect on the variation in milk FA composition.

The analysis of desaturation activity indicators highlighted a significant effect of the SCD polymorphism only on the C14:1/C14 ratio, with homozygous AA cows having the highest value (Table 4). The absence of a relationship between SCD genotype and the other FA ratios could be ascribed to the wide range of factors influencing desaturation activity of the mammary gland such as differential uptake, use, and turnover of the different FA (Bernard et al., 2006). On the other hand, the C14:1/C14 ratio has been suggested as the best indicator for the SCD activity (Corl et al., 2001; Lock and Garnsworthy, 2003): C14:0 in milk fat derives almost exclusively from de novo synthesis in the mammary gland, and therefore, almost all the cis-9 C14:1 is likely to be synthesized by SCD (Bernard et al., 2006).

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

	ACKNOWLEDGEMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Research supported by the Italian Ministero dell’Università e della Ricerca Scientifica (COFIN 2003). The authors acknowledge Adrian Wallwork (University of Pisa, Italy) for his critical reading of the manuscript.

Received for publication September 21, 2006. Accepted for publication May 15, 2007.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 


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