Genotypic and nutritional regulation of gene expression in two sheep hindlimb muscles with distinct myofibre and metabolic characteristics
G. S. Nattrass A D , S. P. Quigley A , G. E. Gardner C , C. S. Bawden A , C. J. McLaughlan A , R. S. Hegarty B and P. L. Greenwood BAustralian Sheep Industry Cooperative Research Centre, Armidale, NSW 2350, Australia.
A South Australian Research and Development Institute—Livestock Systems, Roseworthy, SA 5371, Australia.
B NSW Department of Primary Industries Beef Industry Centre of Excellence, University of New England, Armidale, NSW 2351, Australia.
C School of Rural Science and Natural Resources, University of New England, Armidale, NSW 2351, Australia; Present address: School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, WA 6150, Australia.
D Corresponding author. Email: nattrass.greg@saugov.sa.gov.au
Australian Journal of Agricultural Research 57(6) 691-698 https://doi.org/10.1071/AR05101
Submitted: 21 March 2005 Accepted: 10 May 2006 Published: 20 June 2006
Abstract
This study investigated whether the expression profile of GDF8 (myostatin), myogenic regulatory factors (MRFs: MYF5, MYOD1, MYOG (myogenin), and MYF6), and IGF-system (IGF1, IGF2, IGF1R) genes are correlated with anatomical muscle, nutrition level, and estimated breeding values (EBVs) for muscling, growth, and/or fatness. Real-time PCR was employed to quantitatively measure the mRNA levels of these genes in the semimembranosus (SM) and semitendinosus (ST) muscles of growing lambs. The lambs were sired by Poll Dorset rams with differing EBVs for growth, muscling, and fatness, and were fed either high or low quality and availability pasture from birth to ~8 months of age. With the exception of MYOD1, the mRNA levels of all genes examined in this study showed varying degrees of nutritional regulation. All the MRF mRNA levels were higher in the SM muscle than the ST muscle, whereas myostatin mRNA was higher in the ST muscle than the SM muscle. Interactions between muscle type and nutrition were detected for IGF2, MYF6, and myogenin, while positive correlations between IGF2 and IGF1R and between MYOD1 and myogenin mRNA levels were apparent in both muscles. At the genotypic level, subtle differences in mRNA levels suggested interactions between nutrition and sire EBV. The findings of this study confirm that the MRFs, IGFs, and myostatin genes are differentially affected by a variety of factors that include nutrition, muscle type, and sire EBVs. Together, these data suggest that this suite of genes has important roles during postnatal muscle growth, even at quite late stages of growth and development.
Additional keywords: myogenic regulatory factors, myostatin, insulin-like growth factors, satellite cells, estimated breeding values.
Acknowledgments
We would like to thank the Australian Sheep Industry Cooperative Research Centre for providing the funds to conduct this research and to Meat and Livestock Australia (MLA) for funding the original Management Solutions experiment, which provided the muscle samples used in our study. We also thank the following technicians, Reg Woodgate, Joe Brunner, Bill Johns, and Steve Sinclair from the NSW Department of Primary Industries Beef Industry Centre of Excellence, who helped manage the nutritional requirements of the sheep and collect the muscle biopsy samples prior to slaughter. We also wish to acknowledge the considerable inputs of Dr David Hopkins in providing constructive criticisms and suggestions during the development and revision of this paper.
Buckingham M,
Bajard L,
Chang T,
Daubas P,
Hadchouel J,
Meilhac S,
Montarras D,
Rocancourt D, Relaix F
(2003) The formation of skeletal muscle: from somite to limb. Journal of Anatomy 202, 59–68.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Carlson CJ,
Booth FW, Gordon SE
(1999) Skeletal muscle myostatin mRNA expression is fibre-type specific and increases during hindlimb unloading. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 277, R601–R606.
Cornelison DDW, Wold BJ
(1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Developmental Biology 191, 270–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dedkov EI,
Kostrominova TY,
Borisov AB, Carlson BM
(2003) MyoD and myogenin protein expression in skeletal muscles of senile rats. Cell and Tissue Research 311, 401–416.
| PubMed |
Ekmark M,
Gronevik E,
Schjerling P, Gundersen K
(2003) Myogenin induces higher oxidative capacity in pre-existing mouse muscle fibres after somatic DNA transfer. Journal of Physiology 548, 259–269.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Florini JR,
Ewton DZ, Coolican SA
(1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocrine Reviews 17, 481–517.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gardner GE,
Jacobs RH, Pethick DW
(2001) The effect of magnesium oxide supplementation on muscle glycogen metabolism before and after exercise and at slaughter in sheep. Australian Journal of Agricultural Research 52, 723–729.
| Crossref | GoogleScholarGoogle Scholar |
Gardner GE,
Pethick DW,
Greenwood PL, Hegarty RS
(2006) The effect of genotype and plane of nutrition on the rate of pH decline in lamb carcasses and the expression of metabolic enzymatic markers. Australian Journal of Agricultural Research 57, 661–670.
Greenwood PL,
Davis JJ,
Gaunt GM, Ferrier GR
(2006a) Influences on the loin and cellular characteristics of the m. longissimus lumborum of Australian Poll Dorset-sired lambs. Australian Journal of Agricultural Research 57, 1–12.
| Crossref | GoogleScholarGoogle Scholar |
Greenwood PL,
Gardner GE, Hegarty RS
(2006b) Lamb myofibre characteristics are influenced by sire estimated breeding values and pastoral nutritional system. Australian Journal of Agricultural Research 57, 627–639.
| Crossref |
Greenwood PL,
Gardner GE, Hegarty RS
(2006c) Indices of cellular development in muscles of lambs are influenced by sire estimated breeding values and pastoral nutritional system. Australian Journal of Agricultural Research 57, 651–659.
| Crossref |
Greenwood PL,
Hunt AS,
Slepetis RM,
Finnerty KD,
Alston C,
Beerman DH, Bell AW
(2002) Effects of birth weight and postnatal nutrition on neonatal sheep: III. Regulation of energy metabolism. Journal of Animal Science 80, 2850–2861.
| PubMed |
Grounds MD,
Garrett KL,
Lai MC,
Wright WE, Beilharz MW
(1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell and Tissue Research 267, 99–104.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guernec A,
Berri C,
Chevalier B,
Wacrenier-Cere N,
Le Bihan-Duval E, Duclos MJ
(2003) Muscle development, insulin-like growth factor-I and myostatin mRNA levels in chickens selected for increased breast muscle yield. Growth Hormone & IGF Research 13, 8–18.
| Crossref | GoogleScholarGoogle Scholar |
Hegarty RS,
Hopkins DL,
Farrell TC,
Banks R, Harden S
(2006b) Effects of available nutrition and sire breeding values for growth and muscling on the development of crossbred lambs. 2: Composition and commercial yield. Australian Journal of Agricultural Research 57, 617–626.
Hegarty RS,
Shands C,
Marchant R,
Hopkins DL,
Ball AJ, Harden S
(2006a) Effects of available nutrition and sire breeding values for growth and muscling on the development of crossbred lambs. 1: Growth and carcass characteristics. Australian Journal of Agricultural Research 57, 593–603.
Hegarty RS,
McFarlane JR,
Banks R, Harden S
(2006c) Association of plasma metabolites and hormones with the growth and composition of lambs as affected by nutrition and sire genetics. Australian Journal of Agricultural Research 57, 683–690.
Hughes SM,
Chi MM-Y,
Lowry OH, Gundersen K
(1999) Myogenin induces a shift of enzyme activity from glycolytic to oxidative metabolism in muscles of transgenic mice. Journal of Cell Biology 145, 633–642.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hughes SM,
Koishi K,
Rudnicki M, Maggs AM
(1997) MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mechanisms of Development 61, 151–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hyatt JP,
Roy RR,
Baldwin KM, Edgerton VR
(2003) Nerve activity-independent regulation of skeletal muscle atrophy: role of MyoD and myogenin in satellite cells and myonuclei. American Journal of Physiology – Cell Physiology 285, C1161–C1173.
| PubMed |
Jacobs-El J,
Zhou MY, Russell B
(1995) MRF4, Myf-5, and myogenin mRNAs in the adaptive responses of mature rat muscle. American Journal of Physiology 268, 1045–1052.
Jeanplong J,
Bass JJ,
Smith HK,
Kirk SP,
Kambadur R,
Sharma M, Oldham JM
(2003) Prolonged underfeeding of sheep increases myostatin and myogenic regulatory factor Myf-5 in skeletal muscle while IGF-1 and myogenin are repressed. Journal of Endocrinology 176, 425–437.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kawada S,
Tachi C, Ishii N
(2001) Content and localization of myostatin in mouse skeletal muscles during aging, mechanical unloading and reloading. Journal of Muscle Research and Cell Motility 22, 627–633.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Langley B,
Thomas M,
Bishop A,
Sharma M,
Gilmour S, Kambadur R
(2002) Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. Journal of Biological Chemistry 277, 49831–49840.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lowe DA,
Lund T, Alway SE
(1998) Hypertrophy-stimulated myogenic regulatory factor mRNA increases are attenuated in fast muscle of aged quails. American Journal of Physiology – Cell Physiology 275, C155–C162.
McCroskery S,
Thomas M,
Maxwell L,
Sharma M, Kambadur R
(2003) Myostatin negatively regulates satellite cell activation and self-renewal. Journal of Cell Biology 162, 1135–1147.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McPherron AC,
Lawler AM, Lee SJ
(1997a) Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387, 83–90.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mott I, Ivarie R
(2002) Expression of myostatin is not altered in lines of poultry exhibiting myoblast hyper- and hypo-plasia. Poultry Science 81, 799–804.
| PubMed |
Musaro A,
Cusella De Angelis MG,
Germani A,
Ciccarelli C,
Molinaro M, Zani BM
(1995) Enhanced expression of myogenic regulatory genes in aging skeletal muscle. Experimental Cell Research 221, 241–248.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pownall ME,
Gustafsson MK, Emerson CP
(2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annual Review of Cell and Developmental Biology 18, 747–783.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rupp RA,
Singhal N, Veenstra GJC
(2002) When the embryonic genome flexes its muscles – Chromatin and myogenic transcription regulation. European Journal of Biochemistry 269, 2294–2299.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Salerno MS,
Thomas M,
Forbes D,
Watson T,
Kambadur R, Sharma M
(2004) Molecular analysis of fiber type-specific expression of murine myostatin promoter. American Journal of Physiology – Cell Physiology 287, C1031–C1040.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Siu PM,
Donley DA,
Bryner RW, Alway SE
(2004) Myogenin and oxidative enzyme gene expression levels are elevated in rat soleus muscles after endurance training. Journal of Applied Physiology 97, 277–285.
| PubMed |
te Pas MF,
Verburg FJ,
Gerritsen CL, de Greef KH
(2000) Messenger ribonucleic acid expression of the MyoD gene family in muscle tissue at slaughter in relation to selection for porcine growth rate. Journal of Animal Science 78, 69–77.
| PubMed |
Walters EH,
Stickland NC, Loughna PT
(2000) MRF-4 exhibits fibre type- and muscle-specific pattern of expression in postnatal rat muscle. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 278, R1381–R1384.
| PubMed |
Wigmore PM, Evans DJ
(2002) Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. International Review of Cytology 216, 175–232.
| PubMed |
Yang SY, Goldspink G
(2002) Different roles of the IGF-IEc peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Letters 522, 156–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |