Variation in protein abundance profiles in the M. semitendinosus of lambs bred from sires selected on the basis of growth and muscling potential
M. B. McDonagh A E , K. L. Ferguson B , A. Bacic B , G. E. Gardner C and R. S. Hegarty DA Victorian Department of Primary Industries, Werribee, Vic. 3030, Australia.
B Australian Centre for Plant Functional Genomics and Plant Cell Biology Research Centre, School of Botany, The University of Melbourne, Vic. 3010, Australia.
C University of New England, Armidale, NSW 2351, Australia.
D NSW Department of Primary Industries, Beef Industry Centre of Excellence, Armidale, NSW 2351, Australia.
E Corresponding author. Email: Matthew.McDonagh@dpi.vic.gov.au
Australian Journal of Agricultural Research 57(6) 671-682 https://doi.org/10.1071/AR04277
Submitted: 16 November 2004 Accepted: 7 December 2005 Published: 20 June 2006
Abstract
Relative abundance of proteins localised in the nuclear-enriched, total cell membrane and cytosolic fractions of the semitendinosus muscle was compared between lambs bred from control (C), high muscling (M), and high growth rate (G) sires. In total, 31 proteins were identified whose abundance was differentially regulated between sire type. Differences in hind-limb muscle development between M lambs and C and G lambs were reflected in levels of proteins that regulate or function in cellular mechanisms of protein and energy metabolism. Despite no apparent difference in hind-limb muscle growth in G lambs compared to C, G lambs exhibited marked differences in proteins involved in regulation and function of energy metabolism. These results detail pathways that can be specifically targeted to enhance muscle accretion and growth in lambs. The development of means to manipulate these cellular mechanisms may yield greater gains in muscle accretion and growth rate than breeding on the basis for genetic capacity alone.
Additional keywords: proteomics, proteome, skeletal muscle, sheep, expression, two-dimensional electrophoresis.
Acknowledgments
The authors are grateful for the technical assistance provided by Dete Hasse, Matthew Kerr, and Peter Walker. This research was funded by the Department of Primary Industries Victoria, The Australian Sheep Industry Cooperative Research Centre, and Meat and Livestock Australia. Antony Bacic acknowledges support received from the Victorian State government STII funding to the Victorian Centre for Plant Functional Genomics. Kris Ferguson is supported by funding from the ARC and GRDC to the Australian Centre for Plant Functional Genomics. The authors thank Dr V. H. Oddy for his constructive comment and critical review of this manuscript.
Berggren KN,
Schulenberg B,
Lopez MF,
Steinberg TH,
Bogdanove A,
Smejkal G,
Wang A, Patton WF
(2002) An improved formulation of SYPRO Ruby protein gel stain: Comparison with the original formulation and with a ruthenium II tris (bathophenanthroline disulfonate) formulation. Proteomics 2, 486–498.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brown S,
McGrath MJ,
Ooms LM,
Gurung R,
Maimone MM, Mitchell CA
(1999) Characterization of two isoforms of the skeletal muscle LIM protein 1, SLIM1. Localization of SLIM1 at focal adhesions and the isoform slimmer in the nucleus of myoblasts and cytoplasm of myotubes suggests distinct roles in the cytoskeleton and in nuclear-cytoplasmic communication. Journal of Biological Chemistry 274, 27083–27091.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Capeau J
(2004) Insulin signaling: mechanisms altered in insulin resistance. Médecine Sciences 19, 834–839.
Cartaud A,
Jasmin BJ,
Changeux JP, Cartaud J
(1995) Direct involvement of a lamin-B-related (54 kDa) protein in the association of intermediate filaments with the postsynaptic membrane of the Torpedo marmorata electrolyte. Journal of Cell Science 108, 153–160.
| PubMed |
Chen EH,
Pryce BA,
Tzeng JA,
Gonzalez GA, Olson EN
(2003) Control of myoblast fusion by a guanine nucleotide exchange factor, loner, and its effector ARF6. Cell 114, 751–762.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Choi CS,
Kim YB,
Lee FN,
Zabolotny JM,
Kahn BB, Youn JH
(2002) Lactate induces insulin resistance in skeletal muscle by suppressing glycolysis and impairing insulin signaling. American Journal of Physiology 283, E233–E240.
| PubMed |
Costa ML,
Escaleira R,
Cataldo A,
Oliveira F, Mermelstein CS
(2004) Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Brazilian Journal of Medical and Biological Research 37, 1819–1830.
| PubMed |
Delgado EF,
Geesink GH,
Marchello JA,
Goll DE, Koohmaraie M
(2001) The calpain system in three muscles of normal and callipyge sheep. Journal of Animal Science 79, 398–412.
| PubMed |
Dorow DS,
Devereux L,
Dietzsch E, De Kretser T
(1993) Identification of a new family of human epithelial protein kinases containing two leucine/isoleucine-zipper domains. European Journal of Biochemistry 213, 701–710.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Drinkwater CC,
Evans BA, Richards RI
(1987) Mouse glandular kallikrein genes: identification and characterization of the genes encoding the epidermal growth factor binding proteins. Biochemistry 26, 6750–6756.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Evans BA,
Drinkwater CC, Richards R
(1987) Mouse glandular kallikrein genes. Structure and partial sequence analysis of the kallikrein gene locus. Journal of Biological Chemistry 262, 8027–8034.
| PubMed |
Fearnley IM,
Runswick MJ, Walker JE
(1989) A homologue of the nuclear coded 49 kd subunit of bovine mitochondrial NADH-ubiquinone reductase is coded in chloroplast DNA. EMBO Journal 8, 665–672.
| PubMed |
Furukawa K, Hotta Y
(1993) cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO Journal 12, 97–106.
| PubMed |
Gardner GE,
Jacob RHA, 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 |
Greenwood PL,
Gardner GE, Hegarty RS
(2006) Lamb myofibre characteristics are influenced by sire estimated breeding values and pastoral nutritional system. Australian Journal of Agricultural Research 57, 627–639.
| Crossref |
Hahn Y,
Lee J,
Seong C,
Yoon J, Chung JH
(1999) Structural analysis of phylogenetically conserved J domain protein gene. Biochimica et Biophysica Acta 1447, 325–333.
| PubMed |
Hall DG,
Fogarty NM,
Holst PJ,
Gilmour AR,
Banks R, Luff AF
(1992) Growth and carcase fatness of ewe lambs sired by rams with different LAMBPLAN estimated breeding values. Proceedings of the Australian Association of Animal Breeding and Genetics 10, 316–319.
Hall DG,
Gilmour AR,
Fogarty NM, Holst PJ
(2002) Growth and carcass composition of second-cross lambs. 2. Relationship between estimated breeding values of sires and their progeny performance under fast and slow growth regimes. Australian Journal of Agricultural Research 53, 1341–1348.
| Crossref | GoogleScholarGoogle Scholar |
Hatzfeld M,
Kristjansson GI,
Plessmann U, Weber K
(1994) Band 6 protein, a major constituent of desmosomes from stratified epithelia, is a novel member of the armadillo multigene family. Journal of Cell Science 107, 2259–2270.
| PubMed |
Hatzfeld M, Nachtsheim C
(1996) Cloning and characterization of a new armadillo family member, p0071, associated with the junctional plaque: evidence for a subfamily of closely related proteins. Journal of Cell Science 109, 2767–2778.
| PubMed |
Hegarty RS,
Hopkins DL,
Farrell TC,
Banks R, Harden S
(2006) 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.
Hess JF,
Casselman JT, Fitzgerald PG
(1994) Nucleotide sequence of the bovine vimentin-encoding cDNA. Gene 140, 257–259.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kimball SR,
O'Malley JP,
Anthony JC,
Crozier SJ, Jefferson LS
(2004) Assessment of biomarkers of protein anabolism in skeletal muscle during the life span of the rat: sarcopenia despite elevated protein synthesis. American Journal of Physiology, Endocrinology and Metabolism 287, E772–E780.
| Crossref | GoogleScholarGoogle Scholar |
Koistinen HA, Zierath JR
(2002) Regulation of glucose transport in human skeletal muscle. Annals of Medicine 34, 410–418.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koohmaraie M,
Shackelford SD,
Wheeler TL,
Lonergan SM, Doumit ME
(1995) A muscle hypertrophy condition in lamb (callipyge): Characterisation of effects on muscle growth and meat quality traits. Journal of Animal Science 73, 3596–3607.
| PubMed |
Kreft SG, Nassal M
(2003) hRUL138, a novel human RNA-binding RING-H2 ubiquitin-protein ligase. Journal of Cell Science 116, 605–616.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee YS,
Marks AR,
Gureckas N,
Lacro R,
Nadal-Ginard B, Kim DH
(1992) Purification, characterization, and molecular cloning of a 60-kDa phosphoprotein in rabbit skeletal sarcoplasmic reticulum which is an isoform of phosphoglucomutase. Journal of Biological Chemistry 267, 21080–21088.
| PubMed |
Li H,
Choudhary SK,
Milner DJ,
Munir MI,
Kuisk IR, Capetanaki Y
(1994) Inhibition of desmin expression blocks myoblast fusion and interferes with the myogenic regulators MyoD and myogenin. The Journal of Cell Biology 124, 827–841.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Locke M,
Atkinson BG,
Tanguay RM, Noble EG
(1994) Shifts in type I fiber proportion in rat hindlimb muscle are accompanied by changes in HSP72 content. American Journal of Physiology 266, C1240–C1246.
| PubMed |
Long YC,
Widegren U, Zierath JR
(2004) Exercise-induced mitogen-activated protein kinase signalling in skeletal muscle. Proceedings of the Nutrition Society 63, 227–232.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lorenzen CL,
Koohmaraie M,
Shackelford SD,
Jahoor F,
Freetly HC,
Wheeler TL,
Savell JW, Fiorotto ML
(2000) Protein kinetics in callipyge lambs. Journal of Animal Science 78, 78–87.
| PubMed |
Matecki S,
Py G,
Lambert K,
Peyreigne C,
Mercier J,
Prefaut C, Ramonatxo M
(2002) Effect of prolonged undernutrition on rat diaphragm mitochondrial respiration. American Journal of Respiratory Cell and Molecular Biology 26, 239–245.
| PubMed |
McDonagh MB,
Fernandez C, Oddy VH
(1999) Hind-limb protein metabolism and calpain system activity influence post-mortem change in meat quality in lamb. Meat Science 52, 9–18.
| Crossref | GoogleScholarGoogle Scholar |
Memon AR
(2004) The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochimica et Biophysica Acta 1664, 9–30.
| PubMed |
Nagase T,
Ishikawa K-I,
Suyama M,
Kikuno R,
Hirosawa M,
Miyajima N,
Tanaka A,
Kotani H,
Nomura N, Ohara O
(1999) Prediction of the coding sequences of unidentified human genes. XIII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Research 6, 63–70.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Oddy VH
(1993) Regulation of muscle protein metabolism in sheep and lambs: nutritional, endocrine and genetic aspects. Australian Journal of Agricultural Research 44, 901–913.
| Crossref | GoogleScholarGoogle Scholar |
Oddy VH,
Herd RM,
McDonagh MB,
Woodgate R,
Quinn CA, Zirkler K
(1998) Effect of divergent selection for yearling growth rate on protein metabolism in hind-limb and whole body of Angus cattle. Livestock Production Science 56, 225–231.
| Crossref | GoogleScholarGoogle Scholar |
O’Farrell PH
(1975) High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250, 4007–4021.
| PubMed |
Olson EN,
Brennan TJ,
Chakraborty T,
Cheng TC,
Csejesi P,
Edmondson D,
James G, Li L
(1991) Molecular control of myogenesis: antagonism between growth and differentiation. Molecular and Cellular Biochemistry 104, 7–13.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
O’Neill DE, Noble EG
(2004) Constitutive expression of inducible Hsp70 is linked to natural shifts in skeletal muscle phenotype. Acta Physiologica Scandinavica 181, 35–41.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pathak VK,
Nielsen PJ,
Trachsel H, Hershey JW
(1988) Structure of the beta subunit of translational initiation factor eIF-2. Cell 54, 633–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pestov DG,
Grzeszkiewicz TM, Lau LF
(1998) Isolation of growth suppressors from a cDNA expression library. Oncogene 17, 3187–3197.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rivera AA,
Elton TS,
Dey NB,
Bounelis P, Marchase RB
(1993) Isolation and expression of a rat liver cDNA encoding phosphoglucomutase. Gene 133, 261–266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sato T,
Saito H,
Swensen J,
Olifant A, Wood C , et al.
(1992) The human prohibitin gene located on chromosome 17q21 is mutated in sporadic breast cancer. Cancer Research 52, 1643–1646.
| PubMed |
Srinivasan S,
Traini M,
Herbert B,
Sexton D,
Harry J,
Alexander H,
Williams KL, Alexander S
(2001) Proteomic analysis of a developmentally regulated secretory vesicle. Proteomics 1, 1119–1127.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stayner CK, Tweedie JW
(1995) Cloning and characterisation of the cDNA for sheep liver cytosolic aldehyde dehydrogenase. Advances in Experimental Medicine and Biology 372, 61–66.
| PubMed |
Strausberg RL,
Feingold EA,
Grouse LH,
Derge JG, Klausner RD , et al..
(2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proceedings of the National Academy of Sciences of the United States of America 99, 16899–16903.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Strezoska Z,
Pestov DG, Lau LF
(2002) Functional inactivation of the mouse nuceolar protein Bop1 inhibits multiple steps in pre-mRNA processing and blocks cell cycle progression. Journal of Biological Chemistry 277, 29617–29625.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sun L,
Liu L,
Yang X, Wu Z
(2004) Akt binds prohibitin 2 and relieves its repression of MyoD and muscle differentiation. Journal of Cell Science 117, 3021–3029.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Suttle DP,
Bugg BY,
Winkler JK, Kanalas JJ
(1988) Molecular cloning and nucleotide sequence for the complete coding region of human UMP synthase. Proceedings of the National Academy of Sciences of the United States of America 85, 1754–1758.
| Crossref |
PubMed |
Taniguchi Y,
Furukawa T,
Tun T,
Han H, Honjo T
(1998) LIM protein KyoT2 negatively regulates transcription by association with the RBP-J DNA-binding protein. Molecular and Cellular Biology 18, 644–654.
| PubMed |
Vaittinen S,
Lukka R,
Sahlgren C,
Hurme T,
Rantanen J,
Lendahl U,
Eriksson JE, Kalimo H
(2001) The expression of intermediate filament protein nestin as related to vimentin and desmin in regenerating skeletal muscle. Journal of Neuropathology and Experimental Neurology 60, 588–597.
| PubMed |
Volonte D,
Galbiati F,
Li S,
Nishiyama K,
Okamoto T, Lisanti MP
(1999) Flotillins/cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. Journal of Biological Chemistry 274, 12702–12709.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Warner JR
(1999) The economics of ribosome biosynthesis in yeast. Trends in Biochemical Sciences 24, 437–440.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
York JD, Majerus PW
(1990) Isolation and heterologous expression of a cDNA encoding bovine inositol polyphosphate 1-phosphatase. Proceedings of the National Academy of Sciences of the United States of America 87, 9548–9552.
| Crossref |
PubMed |
