Residual feed intake phenotype and gender affect the expression of key genes of the lipogenesis pathway in subcutaneous adipose tissue of beef cattle
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摘要
Background: Feed accounts for up to 75% of costs in beef production systems,thus any improvement in feed efficiency(FE) will benefit the profitability of this enterprise.Residual feed intake(RFI) is a measure of FE that is independent of level of production.Adipose tissue(AT) is a major endocrine organ and the primary metabolic energy reservoir.It modulates a variety of processes related to FE such as lipid metabolism and glucose homeostasis and thus measures of inter-animal variation in adiposity are frequently included in the calculation of the RFI index.The aim of this study was to determine the effect of phenotypic RFI status and gender on the expression of key candidate genes related to processes involved in energy metabolism within AT.Dry matter intake(DMI) and average daily gain(ADG) were measured over a period of 70 d for 52 purebred Simmental heifers(n = 24) and bulls(n = 28) with an initial BW±SD of 372±39.6 kg and 387±50.6 kg,respectively.Residual feed intake was calculated and animals were ranked within gender by RFI into high(inefficient; n = 9 heifers and n = 8 bulls)and low(efficient; n = 9 heifers and n = 8 bulls) groups.Results: Average daily gain ±SD and daily DMI ±SD for heifers and bul s were 1.2±0.4 kg and 9.1±0.5 kg,and 1.8±0.3 kg and 9.5±1 kg respectively.High RFI heifers and bulls consumed 10% and 15% more(P < 0.05) than their low RFI counterparts,respectively.Heifers had a higher expression of all genes measured than bulls(P < 0.05).A gender × RFI interaction was detected for HMGCS2(P < 0.05) in which high RFI bulls tended to have lower expression of HMGCS2 than low RFI bulls(P < 0.1),whereas high RFI heifers had higher expression than low RFI heifers(P < 0.05) and high RFI bulls(P < 0.05).SLC2 A4 expression was consistently higher in subcutaneous AT of low RFI animals across gender.Conclusion: The findings of this study indicate that low RFI cattle exhibit upregulation of the molecular mechanisms governing glucose metabolism in adipose tissue,in particular,glucose clearance.The decreased expression of SLC2 A4 in the inefficient cattle may result in less efficient glucose metabolism in these animals.We conclude that SLC2 A4 may be a potential biomarker for RFI in cattle.
Background: Feed accounts for up to 75% of costs in beef production systems,thus any improvement in feed efficiency(FE) will benefit the profitability of this enterprise.Residual feed intake(RFI) is a measure of FE that is independent of level of production.Adipose tissue(AT) is a major endocrine organ and the primary metabolic energy reservoir.It modulates a variety of processes related to FE such as lipid metabolism and glucose homeostasis and thus measures of inter-animal variation in adiposity are frequently included in the calculation of the RFI index.The aim of this study was to determine the effect of phenotypic RFI status and gender on the expression of key candidate genes related to processes involved in energy metabolism within AT.Dry matter intake(DMI) and average daily gain(ADG) were measured over a period of 70 d for 52 purebred Simmental heifers(n = 24) and bulls(n = 28) with an initial BW±SD of 372±39.6 kg and 387±50.6 kg,respectively.Residual feed intake was calculated and animals were ranked within gender by RFI into high(inefficient; n = 9 heifers and n = 8 bulls)and low(efficient; n = 9 heifers and n = 8 bulls) groups.Results: Average daily gain ±SD and daily DMI ±SD for heifers and bul s were 1.2±0.4 kg and 9.1±0.5 kg,and 1.8±0.3 kg and 9.5±1 kg respectively.High RFI heifers and bulls consumed 10% and 15% more(P < 0.05) than their low RFI counterparts,respectively.Heifers had a higher expression of all genes measured than bulls(P < 0.05).A gender × RFI interaction was detected for HMGCS2(P < 0.05) in which high RFI bulls tended to have lower expression of HMGCS2 than low RFI bulls(P < 0.1),whereas high RFI heifers had higher expression than low RFI heifers(P < 0.05) and high RFI bulls(P < 0.05).SLC2 A4 expression was consistently higher in subcutaneous AT of low RFI animals across gender.Conclusion: The findings of this study indicate that low RFI cattle exhibit upregulation of the molecular mechanisms governing glucose metabolism in adipose tissue,in particular,glucose clearance.The decreased expression of SLC2 A4 in the inefficient cattle may result in less efficient glucose metabolism in these animals.We conclude that SLC2 A4 may be a potential biomarker for RFI in cattle.
Background: Feed accounts for up to 75% of costs in beef production systems,thus any improvement in feed efficiency(FE) will benefit the profitability of this enterprise.Residual feed intake(RFI) is a measure of FE that is independent of level of production.Adipose tissue(AT) is a major endocrine organ and the primary metabolic energy reservoir.It modulates a variety of processes related to FE such as lipid metabolism and glucose homeostasis and thus measures of inter-animal variation in adiposity are frequently included in the calculation of the RFI index.The aim of this study was to determine the effect of phenotypic RFI status and gender on the expression of key candidate genes related to processes involved in energy metabolism within AT.Dry matter intake(DMI) and average daily gain(ADG) were measured over a period of 70 d for 52 purebred Simmental heifers(n = 24) and bulls(n = 28) with an initial BW±SD of 372±39.6 kg and 387±50.6 kg,respectively.Residual feed intake was calculated and animals were ranked within gender by RFI into high(inefficient; n = 9 heifers and n = 8 bulls)and low(efficient; n = 9 heifers and n = 8 bulls) groups.Results: Average daily gain ±SD and daily DMI ±SD for heifers and bul s were 1.2±0.4 kg and 9.1±0.5 kg,and 1.8±0.3 kg and 9.5±1 kg respectively.High RFI heifers and bulls consumed 10% and 15% more(P < 0.05) than their low RFI counterparts,respectively.Heifers had a higher expression of all genes measured than bulls(P < 0.05).A gender × RFI interaction was detected for HMGCS2(P < 0.05) in which high RFI bulls tended to have lower expression of HMGCS2 than low RFI bulls(P < 0.1),whereas high RFI heifers had higher expression than low RFI heifers(P < 0.05) and high RFI bulls(P < 0.05).SLC2 A4 expression was consistently higher in subcutaneous AT of low RFI animals across gender.Conclusion: The findings of this study indicate that low RFI cattle exhibit upregulation of the molecular mechanisms governing glucose metabolism in adipose tissue,in particular,glucose clearance.The decreased expression of SLC2 A4 in the inefficient cattle may result in less efficient glucose metabolism in these animals.We conclude that SLC2 A4 may be a potential biomarker for RFI in cattle.
引文
1.Richardson E,Herd R.Biological basis for variation in residual feed intake in beef cattle.2.Synthesis of results following divergent selection.Aust J Exp Agric.2004;44(5):431-40.
2.Fitzsimons C,Kenny D,McGee M.In:C.G.Scanes and R.A.Hill,editor.Molecular physiology of feed efficiency in beef cattle,in biology of domestic animals.Boca Raton:CRC Press;2017.
3.Herd R,Arthur P.Physiological basis for residual feed intake.J Anim Sci.2009;87(14_suppl):E64-71.
4.Lawrence P,Kenny DA,Earley B,Crews DH,McGee M.Grass silage intake,rumen and blood variables,ultrasonic and body measurements,feeding behavior,and activity in pregnant beef heifers differing in phenotypic residual feed intake1.J Anim Sci.2011;89(10):3248-61.
5.Fitzsimons C,Kenny DA,Deighton MH,Fahey AG,McGee M.Methane emissions,body composition,and rumen fermentation traits of beef heifers differing in residual feed intake.J Anim Sci.2013;91(12):5789-800.
6.Fitzsimons C,Kenny D,McGee M.Visceral organ weights,digestion and carcass characteristics of beef bulls differing in residual feed intake offered a high concentrate diet.Animal.2014;8(6):949-59.
7.Fitzsimons C,Kenny DA,Waters SM,Earley B,McGee M.Effects of phenotypic residual feed intake on response to a glucose tolerance test and gene expression in the insulin signaling pathway in longissimus dorsi in beef cattle.J Anim Sci.2014;92(10):4616-31.
8.Greathead HMR,Dawson JM,Scollan ND,Buttery PJ.In vivo measurement of lipogenesis in ruminants using[1-14 C]acetate.Br JNutr.2001;86(1):37-44.
9.Rosen ED,Spiegelman BM.Adipocytes as regulators of energy balance and glucose homeostasis.Nature.2006;444(7121):847.
10.Faust IM,Johnson PR,Hirsch J.Surgical removal of adipose tissue alters feeding behavior and the development of obesity in rats.Science.1977;197(4301):393-6.
11.Byrne CJ,Fair S,English AM,Johnston D,Lonergan P,Kenny DA.Effect of milk replacer and concentrate intake on growth rate,feeding behaviour and systemic metabolite concentrations of pre-weaned bull calves of two dairy breeds.Animal.2017;11(9):1531-8.
12.Robelin J.Growth of adipose tissues in cattle;partitioning between depots,chemical composition and cellularity.A review.Livest Prod Sci.1986;14(4):349-64.
13.Arthur PF,Archer JA,Johnston DJ,Herd RM,Richardson EC,Parnell PF.Genetic and phenotypic variance and covariance components for feed intake,feed efficiency,and other postweaning traits in Angus cattle.J Anim Sci.2001;79(11):2805-11.
14.Moraes GFD,Abreu LRA,Ferreira IC,Pereira IG.Genetic analysis of residual feed intake adjusted for fat and carcass and performance traits in a Nellore herd.Ciênc Rural.2017;47(2)
15.Weber C,Hametner C,Tuchscherer A,Losand B,Kanitz E,Otten W,et al.Variation in fat mobilization during early lactation differently affects feed intake,body condition,and lipid and glucose metabolism in high-yielding dairy cows.J Dairy Sci.2013;96:165-80.
16.Fitzsimons C,Kenny DA,Fahey AG,McGee M.Feeding behavior,ruminal fermentation,and performance of pregnant beef cows differing in phenotypic residual feed intake offered grass silage.J Anim Sci.2014;92(5):2170-81.
17.Hill RA,Ahola JK.Feed efficiency interactions with other traits:Growth and product quality.Feed Effic Beef Ind.2012;145-58.
18.Fuente-Martín E,Argente-Arizón P,Ros P,Argente J,Chowen JA.Sex differences in adipose tissue:it is not only a question of quantity and distribution.Adipocyte.2013;2(3):128-34.
19.Gallagher D,Visser M,Sepulveda D,Pierson RN,Harris T,Heymsfield SB.How useful is body mass index for comparison of body fatness across age,sex,and ethnic groups?Am J Epidemiol.1996;143(3):228-39.
20.Eguinoa P,Brocklehurst S,Arana A,Mendizabal JA,Vernon RG,Purroy A.Lipogenic enzyme activities in different adipose depots of Pirenaican and Holstein bulls and heifers taking into account adipocyte size.J Anim Sci.2003;81(2):432-40.
21.Berg RT,Butterfield RM.New concepts of cattle growth.Sydney:Sydney University press;1976.
22.Kempster A,Harrington G.The value of‘fat-corrected’conformation as an indicator of beef carcass composition within and between breeds.Livest Prod Sci.1980;7(4):361-72.
23.Weber KL,Welly BT,Van Eenennaam AL,Young AE,Porto-Neto LR,Reverter A,Rincon G.Identification of gene networks for residual feed intake in Angus cattle using genomic prediction and RNA-seq.PLoSone.2016;11(3):e0152274.
24.Welch CM,Thornton KJ,Murdoch GK,Chapalamadugu KC,Schneider CS,Ahola JK,et al.An examination of the association of serum IGF-Iconcentration,potential candidate genes,and fiber type composition with variation in residual feed intake in progeny of red Angus sires divergent for maintenance energy EPD.J Anim Sci.2013;91(12):5626-36.
25.Lehner R,Quiroga AD.In:Ridgway ND,McLeod RS,editors.Chapter 5-Fatty Acid Handling in Mammalian Cells,in Biochemistry of Lipids,Lipoproteins and Membranes(Sixth Edition).Boston:Elsevier;2016.p.149-84.
26.Huang S,Czech MP.The GLUT4 glucose transporter.Cell Metab.2007;5(4):237-52.
27.Karnieli E,Armoni M.Transcriptional regulation of the insulin-responsive glucose transporter GLUT4 gene:from physiology to pathology.Am JPhysiol Endocrinol Metab.2008;295(1):E38-45.
28.Lacombe VA.Expression and regulation of facilitative glucose transporters in equine insulin-sensitive tissue:from physiology to pathology.ISRN Vet Sci.2014;1-15.https://doi.org/10.1155/2014/409547
29.Garvey WT,Maianu L,Huecksteadt TP,Birnbaum MJ,Molina JM,Ciaraldi TP.Pretranslational suppression of a glucose transporter protein causes insulin resistance in adipocytes from patients with non-insulin-dependent diabetes mellitus and obesity.J Clin Invest.1991;87(3):1072-81.
30.Garvey WT.Glucose transport and NIDDM.Diabetes Care.1992;15(3):396-417.
31.Bell AW,Thompson GE.Free fatty acid oxidation in bovine muscle in vivo:effects of cold exposure and feeding.Am J Physiol Endocrinol Metab.1979;237(4):E309.
32.Baker SD,Szasz JI,Klein TA,Kuber PS,Hunt CW,Glaze JB,et al.Residual feed intake of purebred Angus steers:effects on meat quality and palatability.JAnim Sci.2006;84(4):938-45.
33.Kelly AK,McGee M,Crews DH,Lynch CO,Wylie AR,Evans RD,et al.Relationship between body measurements,metabolic hormones,metabolites and residual feed intake in performancetested pedigree beef bulls.Livest Sci.2011;135(1):8-16.
2.Fitzsimons C,Kenny D,McGee M.In:C.G.Scanes and R.A.Hill,editor.Molecular physiology of feed efficiency in beef cattle,in biology of domestic animals.Boca Raton:CRC Press;2017.
3.Herd R,Arthur P.Physiological basis for residual feed intake.J Anim Sci.2009;87(14_suppl):E64-71.
4.Lawrence P,Kenny DA,Earley B,Crews DH,McGee M.Grass silage intake,rumen and blood variables,ultrasonic and body measurements,feeding behavior,and activity in pregnant beef heifers differing in phenotypic residual feed intake1.J Anim Sci.2011;89(10):3248-61.
5.Fitzsimons C,Kenny DA,Deighton MH,Fahey AG,McGee M.Methane emissions,body composition,and rumen fermentation traits of beef heifers differing in residual feed intake.J Anim Sci.2013;91(12):5789-800.
6.Fitzsimons C,Kenny D,McGee M.Visceral organ weights,digestion and carcass characteristics of beef bulls differing in residual feed intake offered a high concentrate diet.Animal.2014;8(6):949-59.
7.Fitzsimons C,Kenny DA,Waters SM,Earley B,McGee M.Effects of phenotypic residual feed intake on response to a glucose tolerance test and gene expression in the insulin signaling pathway in longissimus dorsi in beef cattle.J Anim Sci.2014;92(10):4616-31.
8.Greathead HMR,Dawson JM,Scollan ND,Buttery PJ.In vivo measurement of lipogenesis in ruminants using[1-14 C]acetate.Br JNutr.2001;86(1):37-44.
9.Rosen ED,Spiegelman BM.Adipocytes as regulators of energy balance and glucose homeostasis.Nature.2006;444(7121):847.
10.Faust IM,Johnson PR,Hirsch J.Surgical removal of adipose tissue alters feeding behavior and the development of obesity in rats.Science.1977;197(4301):393-6.
11.Byrne CJ,Fair S,English AM,Johnston D,Lonergan P,Kenny DA.Effect of milk replacer and concentrate intake on growth rate,feeding behaviour and systemic metabolite concentrations of pre-weaned bull calves of two dairy breeds.Animal.2017;11(9):1531-8.
12.Robelin J.Growth of adipose tissues in cattle;partitioning between depots,chemical composition and cellularity.A review.Livest Prod Sci.1986;14(4):349-64.
13.Arthur PF,Archer JA,Johnston DJ,Herd RM,Richardson EC,Parnell PF.Genetic and phenotypic variance and covariance components for feed intake,feed efficiency,and other postweaning traits in Angus cattle.J Anim Sci.2001;79(11):2805-11.
14.Moraes GFD,Abreu LRA,Ferreira IC,Pereira IG.Genetic analysis of residual feed intake adjusted for fat and carcass and performance traits in a Nellore herd.Ciênc Rural.2017;47(2)
15.Weber C,Hametner C,Tuchscherer A,Losand B,Kanitz E,Otten W,et al.Variation in fat mobilization during early lactation differently affects feed intake,body condition,and lipid and glucose metabolism in high-yielding dairy cows.J Dairy Sci.2013;96:165-80.
16.Fitzsimons C,Kenny DA,Fahey AG,McGee M.Feeding behavior,ruminal fermentation,and performance of pregnant beef cows differing in phenotypic residual feed intake offered grass silage.J Anim Sci.2014;92(5):2170-81.
17.Hill RA,Ahola JK.Feed efficiency interactions with other traits:Growth and product quality.Feed Effic Beef Ind.2012;145-58.
18.Fuente-Martín E,Argente-Arizón P,Ros P,Argente J,Chowen JA.Sex differences in adipose tissue:it is not only a question of quantity and distribution.Adipocyte.2013;2(3):128-34.
19.Gallagher D,Visser M,Sepulveda D,Pierson RN,Harris T,Heymsfield SB.How useful is body mass index for comparison of body fatness across age,sex,and ethnic groups?Am J Epidemiol.1996;143(3):228-39.
20.Eguinoa P,Brocklehurst S,Arana A,Mendizabal JA,Vernon RG,Purroy A.Lipogenic enzyme activities in different adipose depots of Pirenaican and Holstein bulls and heifers taking into account adipocyte size.J Anim Sci.2003;81(2):432-40.
21.Berg RT,Butterfield RM.New concepts of cattle growth.Sydney:Sydney University press;1976.
22.Kempster A,Harrington G.The value of‘fat-corrected’conformation as an indicator of beef carcass composition within and between breeds.Livest Prod Sci.1980;7(4):361-72.
23.Weber KL,Welly BT,Van Eenennaam AL,Young AE,Porto-Neto LR,Reverter A,Rincon G.Identification of gene networks for residual feed intake in Angus cattle using genomic prediction and RNA-seq.PLoSone.2016;11(3):e0152274.
24.Welch CM,Thornton KJ,Murdoch GK,Chapalamadugu KC,Schneider CS,Ahola JK,et al.An examination of the association of serum IGF-Iconcentration,potential candidate genes,and fiber type composition with variation in residual feed intake in progeny of red Angus sires divergent for maintenance energy EPD.J Anim Sci.2013;91(12):5626-36.
25.Lehner R,Quiroga AD.In:Ridgway ND,McLeod RS,editors.Chapter 5-Fatty Acid Handling in Mammalian Cells,in Biochemistry of Lipids,Lipoproteins and Membranes(Sixth Edition).Boston:Elsevier;2016.p.149-84.
26.Huang S,Czech MP.The GLUT4 glucose transporter.Cell Metab.2007;5(4):237-52.
27.Karnieli E,Armoni M.Transcriptional regulation of the insulin-responsive glucose transporter GLUT4 gene:from physiology to pathology.Am JPhysiol Endocrinol Metab.2008;295(1):E38-45.
28.Lacombe VA.Expression and regulation of facilitative glucose transporters in equine insulin-sensitive tissue:from physiology to pathology.ISRN Vet Sci.2014;1-15.https://doi.org/10.1155/2014/409547
29.Garvey WT,Maianu L,Huecksteadt TP,Birnbaum MJ,Molina JM,Ciaraldi TP.Pretranslational suppression of a glucose transporter protein causes insulin resistance in adipocytes from patients with non-insulin-dependent diabetes mellitus and obesity.J Clin Invest.1991;87(3):1072-81.
30.Garvey WT.Glucose transport and NIDDM.Diabetes Care.1992;15(3):396-417.
31.Bell AW,Thompson GE.Free fatty acid oxidation in bovine muscle in vivo:effects of cold exposure and feeding.Am J Physiol Endocrinol Metab.1979;237(4):E309.
32.Baker SD,Szasz JI,Klein TA,Kuber PS,Hunt CW,Glaze JB,et al.Residual feed intake of purebred Angus steers:effects on meat quality and palatability.JAnim Sci.2006;84(4):938-45.
33.Kelly AK,McGee M,Crews DH,Lynch CO,Wylie AR,Evans RD,et al.Relationship between body measurements,metabolic hormones,metabolites and residual feed intake in performancetested pedigree beef bulls.Livest Sci.2011;135(1):8-16.