Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-03T20:58:42.552Z Has data issue: false hasContentIssue false

Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species

Published online by Cambridge University Press:  21 April 2010

M. Bonnet*
Affiliation:
INRA, UR1213 Herbivores Research Unit, F-63122 Saint-Genès-Champanelle, France
I. Cassar-Malek
Affiliation:
INRA, UR1213 Herbivores Research Unit, F-63122 Saint-Genès-Champanelle, France
Y. Chilliard
Affiliation:
INRA, UR1213 Herbivores Research Unit, F-63122 Saint-Genès-Champanelle, France
B. Picard
Affiliation:
INRA, UR1213 Herbivores Research Unit, F-63122 Saint-Genès-Champanelle, France
Get access

Abstract

The lean-to-fat ratio, that is, the relative masses of muscle and adipose tissue, is a criterion for the yield and quality of bovine carcasses and meat. This review describes the interactions between muscle and adipose tissue (AT) that may regulate the dynamic balance between the number and size of muscle v. adipose cells. Muscle and adipose tissue in cattle grow by an increase in the number of cells (hyperplasia), mainly during foetal life. The total number of muscle fibres is set by the end of the second trimester of gestation. By contrast, the number of adipocytes is never set. Number of adipocytes increases mainly before birth until 1 year of age, depending on the anatomical location of the adipose tissue. Hyperplasia concerns brown pre-adipocytes during foetal life and white pre-adipocytes from a few weeks after birth. A decrease in the number of secondary myofibres and an increase in adiposity in lambs born from mothers severely underfed during early pregnancy suggest a balance in the commitment of a common progenitor into the myogenic or adipogenic lineages, or a reciprocal regulation of the commitment of two distinct progenitors. The developmental origin of white adipocytes is a subject of debate. Molecular and histological data suggested a possible transdifferentiation of brown into white adipocytes, but this hypothesis has now been challenged by the characterization of distinct precursor cells for brown and white adipocytes in mice. Increased nutrient storage in fully differentiated muscle fibres and adipocytes, resulting in cell enlargement (hypertrophy), is thought to be the main mechanism, whereby muscle and fat masses increase in growing cattle. Competition or prioritization between adipose and muscle cells for the uptake and metabolism of nutrients is suggested, besides the successive waves of growth of muscle v. adipose tissue, by the inhibited or delayed adipose tissue growth in bovine genotypes exhibiting strong muscular development. This competition or prioritization occurs through cellular signalling pathways and the secretion of proteins by adipose tissue (adipokines) and muscle (myokines), putatively regulating their hypertrophy in a reciprocal manner. Further work on the mechanisms underlying cross-talk between brown or white adipocytes and muscle fibres will help to achieve better understanding as a prerequisite to improving the control of body growth and composition in cattle.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almind, K, Manieri, M, Sivitz, WI, Cinti, S, Kahn, CR 2007. Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice. Proceedings of the National Academy of Sciences of the United States of America 104, 23662371.CrossRefGoogle ScholarPubMed
Alzón, M, Mendizabal, J, Arana, A, Albertí, P, Purroy, A 2007. Adipocyte cellularity in different adipose depots in bulls of seven Spanish breeds slaughtered at two body weights. Animal 1, 261267.CrossRefGoogle ScholarPubMed
Argiles, JM, Lopez-Soriano, J, Almendro, V, Busquets, S, Lopez-Soriano, FJ 2005. Cross-talk between skeletal muscle and adipose tissue: a link with obesity? Medicinal Research Reviews 25, 4965.CrossRefGoogle ScholarPubMed
Artaza, JN, Bhasin, S, Magee, TR, Reisz-Porszasz, S, Shen, R, Groome, NP, Fareez, MM, Gonzalez-Cadavid, NF 2005. Myostatin inhibits myogenesis and promotes adipogenesis in C3H 10T(1/2) mesenchymal multipotent cells. Endocrinology 146, 35473557.CrossRefGoogle ScholarPubMed
Ashmore, C, Parker, W, Stokes, H, Doerr, L 1974. Comparative aspects of muscle fibre types in fetuses of the normal and double muscled cattle. Growth 38, 501506.Google ScholarPubMed
Atit, R, Sgaier, SK, Mohamed, OA, Taketo, MM, Dufort, D, Joyner, AL, Niswander, L, Conlon, RA 2006. Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Developmental Biology 296, 164176.CrossRefGoogle ScholarPubMed
Avram, MM, Avram, AS, James, WD 2007. Subcutaneous fat in normal and diseased states 3. Adipogenesis: from stem cell to fat cell. Journal of the American Academy of Dermatology 56, 472492.CrossRefGoogle ScholarPubMed
Bajard, L, Relaix, F, Lagha, M, Rocancourt, D, Daubas, P, Buckingham, ME 2006. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes & Development 20, 24502464.CrossRefGoogle ScholarPubMed
Bellinge, RHS, Liberles, DA, Iaschi, SP, O’Brien, AA, Tay, GK 2005. Myostatin and its implications on animal breeding: a review. Animal Genetics 36, 16.CrossRefGoogle ScholarPubMed
Bellmann, O, Wegner, J, Teuscher, F, Schneider, F, Ender, K 2004. Muscle characteristics and corresponding hormone concentrations in different types of cattle. Livestock Production Science 85, 4557.CrossRefGoogle Scholar
Berge, P, Geay, Y, Micol, D 1991. Effect of feeds and growth-rate during the growing phase on subsequent performance during the fattening period and carcass composition in young dairy breed bulls. Livestock Production Science 28, 203222.CrossRefGoogle Scholar
Bernard, L, Leroux, C, Chilliard, Y 2008. Expression and nutritional regulation of lipogenic genes in the ruminant lactating mammary gland. Advances in Experimental Medicine and Biology 606, 67108.CrossRefGoogle ScholarPubMed
Berti, L, Gammeltoft, S 1999. Leptin stimulates glucose uptake in C2C12 muscle cells by activation of ERK2. Molecular and Cellular Endocrinology 157, 121130.CrossRefGoogle ScholarPubMed
Billon, N, Monteiro, MC, Dani, C 2008. Developmental origin of adipocytes: new insights into a pending question. Biology of the Cell 100, 563575.CrossRefGoogle ScholarPubMed
Biressi, S, Molinaro, M, Cossu, G 2007. Cellular heterogeneity during vertebrate skeletal muscle development. Developmental Biology 308, 281293.CrossRefGoogle ScholarPubMed
Bispham, J, Gardner, DS, Gnanalingham, MG, Stephenson, T, Symonds, ME, Budge, H 2005. Maternal nutritional programming of fetal adipose tissue development: differential effects on messenger ribonucleic acid abundance for uncoupling proteins and peroxisome proliferator-activated and prolactin receptors. Endocrinology 146, 39433949.CrossRefGoogle ScholarPubMed
Bispham, J, Gopalakrishnan, GS, Dandrea, J, Wilson, V, Budge, H, Keisler, DH, Broughton Pipkin, F, Stephenson, T, Symonds, ME 2003. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 35753585.CrossRefGoogle ScholarPubMed
Blum, JW, Zbinden, Y, Hammon, HM, Chilliard, Y 2005. Plasma leptin status in young calves: effects of pre-term birth, age, glucocorticoid status, suckling, and feeding with an automatic feeder or by bucket. Domestic Animal Endocrinology 28, 119133.CrossRefGoogle ScholarPubMed
Bonnet, M, Cassar-Malek, I, Delavaud, A, Tourret, M, Chilliard, Y, Picard, B 2008. Développement d’un modèle in vitro de culture d’adipocytes bovins pour étudier les interactions entre adipocytes, myoblastes et fibroblastes. Viandes et Produits Carnés (hors série) “12emes Journées Sciences du Muscle et Technologies des Viandes”, 8 et 9 octobre 2008, Tours, pp. 163–164.Google Scholar
Bonnet, M, Faulconnier, Y, Flechet, J, Hocquette, JF, Leroux, C, Langin, D, Martin, P, Chilliard, Y 1998. Messenger RNAs encoding lipoprotein lipase, fatty acid synthase and hormone-sensitive lipase in the adipose tissue of underfed-refed ewes and cows. Reproduction Nutrition Development 38, 297307.CrossRefGoogle ScholarPubMed
Bonnet, M, Faulconnier, Y, Leroux, C, Jurie, C, Cassar-Malek, I, Bauchart, D, Boulesteix, P, Pethick, D, Hocquette, JF, Chilliard, Y 2007. Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black × Angus steers. Journal of Animal Science 85, 28822894.CrossRefGoogle ScholarPubMed
Boone, C, Mourot, J, Gregoire, F, Remacle, C 2000. The adipose conversion process: regulation by extracellular and intracellular factors. Reproduction Nutrition Development 40, 325358.CrossRefGoogle ScholarPubMed
Bosnakovski, D, Mizuno, M, Kim, G, Takagi, S, Okumura, M, Fujinaga, T 2005. Isolation and multilineage differentiation of bovine bone marrow mesenchymal stem cells. Cell & Tissue Research 319, 243253.CrossRefGoogle ScholarPubMed
Bouley, J, Meunier, B, Chambon, C, De Smet, S, Hocquette, JF, Picard, B 2005. Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics 5, 490500.CrossRefGoogle ScholarPubMed
Brameld, JM, Daniel, Z 2008. In utero effects on livestock muscle development and body composition. Australian Journal of Experimental Agriculture 48, 921929.CrossRefGoogle Scholar
Brandstetter, AM, Picard, B, Geay, Y 1998. Muscle fibre characteristics in four muscles of growing bulls – I. Postnatal differentiation. Livestock Production Science 53, 1523.CrossRefGoogle Scholar
Brandt, MM, Keisler, DH, Meyer, DL, Schmidt, TB, Berg, EP 2007. Serum hormone concentrations relative to carcass composition of a random allotment of commercial-fed beef cattle. Journal of Animal Science 85, 267275.CrossRefGoogle ScholarPubMed
Braun, T, Buschhausendenker, G, Bober, E, Tannich, E, Arnold, HH 1989. A novel human-muscle factor related to but distinct from Myod1 induces myogenic conversion in 10t1/2 fibroblasts. EMBO Journal 8, 701709.CrossRefGoogle ScholarPubMed
Bryson-Richardson, RJ, Currie, PD 2008. The genetics of vertebrate myogenesis. Nature Reviews Genetics 9, 632646.CrossRefGoogle ScholarPubMed
Buckingham, M 2007. Skeletal muscle progenitor cells and the role of Pax genes. Comptes Rendus Biologies 330, 530533.CrossRefGoogle ScholarPubMed
Buckingham, M, Relaix, F 2007. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annual Review of Cell and Developmental Biology 23, 645673.CrossRefGoogle ScholarPubMed
Budge, H, Edwards, LJ, McMillen, IC, Bryce, A, Warnes, K, Pearce, S, Stephenson, T, Symonds, ME 2004. Nutritional manipulation of fetal adipose tissue deposition and uncoupling protein 1 messenger RNA abundance in the sheep: differential effects of timing and duration. Biology of Reproduction 71, 359365.CrossRefGoogle ScholarPubMed
Cannon, B, Nedergaard, J 2004. Brown adipose tissue: function and physiological significance. Physiological Reviews 84, 277359.CrossRefGoogle ScholarPubMed
Cassar-Malek, I, Bonnet, M, Chilliard, Y, Picard, B 2006. Cross-talk between myoblasts, adipocytes and fibroblasts during bovine myogenesis. COST Action 925 – the importance of prenatal events for postnatal muscle growth in relation to the quality of muscle based foods. In Proceedings of the 3rd Work Group Meeting, Antalya, Turkey.Google Scholar
Cassar-Malek, I, Passelaigue, F, Bernard, C, Leger, J, Hocquette, J-F 2007. Target genes of myostatin loss-of-function in muscles of late bovine fetuses. BMC Genomics 8, 63.CrossRefGoogle ScholarPubMed
Cassar-Malek, I, Hocquette, JF, Jurie, C, Listrat, A, Jailler, R, Bauchart, D, Briand, Y, Picard, B 2004. Muscle-specific metabolic, histochemical and biochemical responses to a nutritionally induced discontinuous growth path. Animal Science 79, 4959.CrossRefGoogle Scholar
Cassar-Malek, I, Ueda, Y, Bernard, C, Jurie, C, Sudre, K, Listrat, A, Barnola, I, Gentes, G, Leroux, C, Renand, G, Martin, P, Hocquette, JF 2005. Molecular and biochemical muscle characteristics of Charolais bulls divergently selected for muscle growth. In:Indicators of milk and beef quality (ed. JF Hocquette and S Gigli), EAAP Publication 112, pp. 371377. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
Casteilla, L, Dani, C 2006. Adipose tissue-derived cells: from physiology to regenerative medicine. Diabetes & Metabolism 32, 393401.CrossRefGoogle ScholarPubMed
Casteilla, L, Forest, C, Robelin, J, Ricquier, D, Lombet, A, Ailhaud, G 1987. Characterization of mitochondrial-uncoupling protein in bovine fetus and newborn calf. American Journal of Physiology 252, E627E636.Google ScholarPubMed
Casteilla, L, Champigny, O, Bouillaud, F, Robelin, J, Ricquier, D 1989. Sequential changes in the expression of mitochondrial protein mRNA during the development of brown adipose tissue in bovine and ovine species. Sudden occurrence of uncoupling protein mRNA during embryogenesis and its disappearance after birth. Biochemical Journal 257, 665671.CrossRefGoogle ScholarPubMed
Chakrabarty, K, Romans, JR 1972. Lipogenesis in the adipose cells of the bovine (Bos taurus) as related to their intramuscular fat content. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 41, 603615.CrossRefGoogle ScholarPubMed
Chaze, T, Meunier, B, Chambon, C, Jurie, C, Picard, B 2008. In vivo proteome dynamics during early bovine myogenesis. Proteomics 8, 42364248.CrossRefGoogle ScholarPubMed
Chaze, T, Meunier, B, Chambon, C, Jurie, C, Picard, B 2009. Proteome dynamics during contractile and metabolic differentiation of bovine foetal muscle. Animal 3, 9801000.CrossRefGoogle ScholarPubMed
Chelh, I, Meunier, B, Picard, B, Reecy, M, Chevalier, C, Hocquette, J-F, Cassar-Malek, I 2009. Molecular profiles of Quadriceps muscle in myostatin-null mice reveal PI3K and apoptotic pathways as myostatin targets. BMC Genomics 10, 196.CrossRefGoogle ScholarPubMed
Chelikani, PK, Glimm, DR, Kennelly, JJ 2003. Short communication: tissue distribution of leptin and leptin receptor mrna in the bovine. Journal of Dairy Science 86, 23692372.CrossRefGoogle ScholarPubMed
Chilliard, Y 1993. Dietary fat and adipose tissue metabolism in ruminants, pigs, and rodents: a review. Journal of Dairy Science 76, 38973931.CrossRefGoogle ScholarPubMed
Chilliard, Y, Bocquier, F, Doreau, M 1998. Digestive and metabolic adaptations of ruminants to undernutrition, and consequences on reproduction. Reproduction Nutrition Development 38, 131152.CrossRefGoogle ScholarPubMed
Chilliard, Y, Delavaud, C, Bonnet, M 2005. Leptin expression in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domestic Animal Endocrinology 29, 322.CrossRefGoogle ScholarPubMed
Cho, M, Hughes, SM, Karschmizrachi, I, Travis, M, Leinwand, LA, Blau, HM 1994. Fast myosin heavy-chains expressed in secondary mammalian muscle-fibers at the time of their inception. Journal of Cell Science 107, 23612371.CrossRefGoogle ScholarPubMed
Cianzio, DS, Topel, DG, Whitehurst, GB, Beitz, DC, Self, HL 1985. Adipose tissue growth and cellularity: changes in bovine adipocyte size and number. Journal of Animal Science 60, 970976.CrossRefGoogle ScholarPubMed
Cinti, S 2009. Trans differentiation properties of adipocytes in the Adipose Organ. American Journal of Physiological Endocrinology and Metabolism 297, E977E986.CrossRefGoogle Scholar
Cottrell, EC, Ozanne, SE 2008. Early life programming of obesity and metabolic disease. Physiology & Behavior 94, 1728.CrossRefGoogle ScholarPubMed
Crisan, M, Casteilla, L, Lehr, L, Carmona, M, Paoloni-Giacobino, A, Yap, S, Sun, B, Leger, B, Logar, A, Penicaud, L, Schrauwen, P, Cameron-Smith, D, Russell, AP, Peault, B, Giacobino, JP 2008. A reservoir of brown adipocyte progenitors in human skeletal muscle. Stem Cells 26, 24252433.CrossRefGoogle ScholarPubMed
Cusella de Angelis, MG, Molinari, S, Ledonne, A, Coletta, M, Vivarelli, E, Bouche, M, Molinaro, M, Ferrari, S, Cossu, G 1994. Differential response of embryonic and fetal myoblasts to tgf-beta – a possible regulatory mechanism of skeletal-muscle histogenesis. Development 120, 925933.CrossRefGoogle ScholarPubMed
Daniel, ZC, Brameld, JM, Craigon, J, Scollan, ND, Buttery, PJ 2007. Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition. Journal of Animal Science 85, 15651576.CrossRefGoogle ScholarPubMed
Davis, RL, Weintraub, H, Lassar, AB 1987. Expression of a single transfected cdna converts fibroblasts to myoblasts. Cell 51, 9871000.CrossRefGoogle ScholarPubMed
Deveaux, V, Cassar-Malek, I, Picard, P 2001. Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue foetuses. Comparative Biochemistry and Physiology 131, 2129.CrossRefGoogle ScholarPubMed
Dulloo, AG 2008. Thrifty energy metabolism in catch-up growth trajectories to insulin and leptin resistance. Best practice & research. Clinical Endocrinology & Metabolism 22, 155171.Google Scholar
Duris, MP, Renand, G, Picard, B 1999. Genetic variability of foetal bovine myoblasts in primary culture. The Histochemical Journal 31, 753760.CrossRefGoogle ScholarPubMed
Dyck, DJ, Heigenhauser, GJ, Bruce, CR 2006. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiologica (Oxford, England) 186, 516.CrossRefGoogle ScholarPubMed
Eckardt, K, Sell, H, Eckel, J 2008. Novel aspects of adipocyte-induced skeletal muscle insulin resistance. Archives of Physiology and Biochemistry 114, 287298.CrossRefGoogle ScholarPubMed
Eguinoa, P, Brocklehurst, S, Arana, A, Mendizabal, JA, Vernon, RG, Purroy, A 2003. Lipogenic enzyme activities in different adipose depots of Pirenaican and Holstein bulls and heifers taking into account adipocyte size. Journal of Animal Science 81, 432440.CrossRefGoogle ScholarPubMed
Emerson, CP 1990. Myogenesis and development control genes. Current Opinion in Cell Biology 2, 10651076.CrossRefGoogle Scholar
Fahey, AJ, Brameld, JM, Parr, T, Buttery, PJ 2005. The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. Journal of Animal Science 83, 25642571.CrossRefGoogle ScholarPubMed
Faulconnier, Y, Ortigues-Marty, I, Delavaud, C, Dozias, D, Jailler, R, Micol, D, Chilliard, Y 2007. Influence of the diet and grazing on adipose tissue lipogenic activities and plasma leptin in steers. Animal 1, 12631271.CrossRefGoogle ScholarPubMed
Ford, SP, Hess, BW, Schwope, MM, Nijland, MJ, Gilbert, JS, Vonnahme, KA, Means, WJ, Han, H, Nathanielsz, PW 2007. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. Journal of Animal Science 85, 12851294.CrossRefGoogle ScholarPubMed
Forhead, AJ, Fowden, AL 2009. The hungry fetus? Role of leptin as a nutritional signal before birth. The Journal of Physiology 587, 11451152.CrossRefGoogle ScholarPubMed
Freking, BA, Smith, TPL, Leymaster, KA 2004. The callipyge mutation for sheep muscular hypertrophy – genetics, physiology and meat quality. In Muscle development of livestock animals: physiology, genetics and meat quality (ed. MFW te Pas, ME Everts and HP Haagsman), Chapter 15, pp. 317342. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Fruhbeck, G, Sesma, P, Burrell, MA 2009. PRDM16: the interconvertible adipo-myocyte switch. Trends in Cell Biology 19, 141146.CrossRefGoogle ScholarPubMed
Gagnière, H, Picard, B, Geay, Y 1999a. Contractile differentiation of foetal cattle muscles: intermuscular variability. Reproduction Nutrition Development 39, 637655.CrossRefGoogle ScholarPubMed
Gagnière, H, Picard, B, Jurie, C, Geay, Y 1999b. Comparison of foetal metabolic differentiation in three cattle muscles. Reproduction Nutrition Development 39, 105112.CrossRefGoogle ScholarPubMed
Gagnière, H, Ménissier, F, Geay, Y, Picard, B 2000. Influence of genotype on contractile protein differentiation in different bovine muscles during foetal life. Annales de Zootechnie 49, 405423.CrossRefGoogle Scholar
Garbutt, GJ, Anthony, WB, Walker, DF, Mcguire, JA 1979. Peri-rectal adipose-tissue development of post-weaned rapidly growing bull calves. Journal of Animal Science 48, 525530.CrossRefGoogle Scholar
Gardner, DS, Tingey, K, Van Bon, BW, Ozanne, SE, Wilson, V, Dandrea, J, Keisler, DH, Stephenson, T, Symonds, ME 2005. Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. American Journal of Physiology – Regulatory Integrative and Comparative Physiology 289, R947R954.CrossRefGoogle ScholarPubMed
Geay, Y, Robelin, J 1979. Variation of meat production capacity in cattle due to genotype and level of feeding – genotype-nutrition interaction. Livestock Production Science 6, 263276.CrossRefGoogle Scholar
Gettys, TW, Henricks, DM, Schanbacher, BD 1988. An assessment of the relationship between tissue-growth patterns and selected hormone profiles among sex phenotypes in cattle. Animal Production 47, 335343.Google Scholar
Gotoh, T, Albrecht, E, Teuscher, F, Kawabata, K, Sakashita, K, Iwamoto, H, Wegner, J 2009. Differences in muscle and fat accretion in Japanese Black and European cattle. Meat Science 82, 300308.CrossRefGoogle ScholarPubMed
Graugnard, DE, Piantoni, P, Bionaz, M, Berger, LL, Faulkner, DB, Loor, JJ 2009. Adipogenic and energy metabolism gene networks in Longissimus Lumborum during rapid post-weaning growth in Angus and Angus × Simmental cattle fed high-starch or low-starch diets. BMC Genomics 10, 142.CrossRefGoogle ScholarPubMed
Greathead, HM, Dawson, JM, Craigon, J, Sessions, VA, Scollan, ND, Buttery, PJ 2006. Fat and protein metabolism in growing steers fed either grass silage or dried grass. British Journal of Nutrition 95, 2739.CrossRefGoogle ScholarPubMed
Greenwood, PL, Cafe, LM 2007. Prenatal and pre-weaning growth and nutrition of cattle: long-term consequences for beef production. Animal 1, 12831296.CrossRefGoogle ScholarPubMed
Greenwood, PL, Slepetis, RM, Bell, AW 2000. Influences on fetal and placental weights during mid to late gestation in prolific ewes well nourished throughout pregnancy. Reproduction Fertility and Development 12, 149156.CrossRefGoogle ScholarPubMed
Greenwood, PL, Hunt, AS, Hermanson, JW, Bell, AW 1998. Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. Journal of Animal Science 76, 23542367.CrossRefGoogle ScholarPubMed
Greenwood, PL, Slepetis, RM, Hermanson, JW, Bell, AW 1999. Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reproduction Fertility and Development 11, 281291.CrossRefGoogle Scholar
Greenwood, PL, Cafe, LM, Hearnshaw, H, Hennessy, DW, Thompson, JM, Morris, SG 2006. Long-term consequences of birth weight and growth to weaning on carcass, yield and beef quality characteristics of piedmontese- and wagyu-sired cattle. Australian Journal of Experimental Agriculture 46, 257269.CrossRefGoogle Scholar
Greenwood, PL, Tomkins, NW, Hunter, RA, Allingham, PG, Harden, S, Harper, GS 2009. Bovine myofiber characteristics are influenced by postweaning nutrition. Journal of Animal Science 87, 31143123.CrossRefGoogle ScholarPubMed
Gregoire, FM, Smas, CM, Sul, HS 1998. Understanding adipocyte differentiation. Physiological Reviews 78, 783809.CrossRefGoogle ScholarPubMed
Guo, W, Flanagan, J, Jasuja, R, Kirkland, J, Jiang, L, Bhasin, S 2008. The effects of myostatin on adipogenic differentiation of human bone marrow-derived mesenchymal stem cells are mediated through cross-communication between smad3 and wnt/beta-catenin signaling pathways. Journal of Biological Chemistry 283, 91369145.CrossRefGoogle ScholarPubMed
Hasty, P, Bradley, A, Morris, JH, Edmondson, DG, Venuti, JM, Olson, EN, Klein, WH 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501506.CrossRefGoogle ScholarPubMed
Hausman, GJ, Dodson, MV, Ajuwon, K, Azain, M, Barnes, KM, Guan, LL, Jiang, Z, Poulos, SP, Sainz, RD, Smith, S, Spurlock, M, Novakofski, J, Fernyhough, ME, Bergen, WG 2009. Board-invited review: the biology and regulation of preadipocytes and adipocytes in meat animals. Journal of Animal Science 87, 12181246.CrossRefGoogle ScholarPubMed
Hirai, S, Matsumoto, H, Hino, N, Kawachi, H, Matsui, T, Yano, H 2007. Myostatin inhibits differentiation of bovine preadipocyte. Domestic Animal Endocrinology 32, 114.CrossRefGoogle ScholarPubMed
Hocquette, JF, Sauerwein, H, Higashiyama, Y, Picard, B, Abe, H 2006. Prenatal developmental changes in glucose transporters, intermediary metabolism and hormonal receptors related to the igf/insulin-glucose axis in the heart and adipose tissue of bovines. Reproduction Nutrition Development 46, 257272.CrossRefGoogle Scholar
Hood, RL, Allen, CE 1973. Cellularity of bovine adipose tissue. Journal of Lipid Research 14, 605610.CrossRefGoogle ScholarPubMed
Hornick, JL, Van Eenaeme, C, Gqrard, O, Dufrasne, I, Istasse, L 2000. Mechanisms of reduced and compensatory growth. Domestic Animal Endocrinology 19, 121132.CrossRefGoogle ScholarPubMed
Jones, SJ, Starkey, DL, Calkins, CR, Crouse, JD 1990. Myofibrillar protein-turnover in feed-restricted and realimented beef-cattle. Journal of Animal Science 68, 27072715.CrossRefGoogle ScholarPubMed
Jurie, C, Picard, B, Geay, Y 1999. Changes in the metabolic and contractile characteristics of muscle in male cattle between 10 and 16 months of age. Histochemical Journal 31, 117122.CrossRefGoogle ScholarPubMed
Jurie, C, Cassar-Malek, I, Bonnet, M, Leroux, C, Bauchart, D, Boulesteix, P, Pethick, DW, Hocquette, JF 2007. Adipocyte fatty acid-binding protein and mitochondrial enzyme activities in muscles as relevant indicators of marbling in cattle. Journal of Animal Science 85, 26602669.CrossRefGoogle ScholarPubMed
Kajimura, S, Seale, P, Tomaru, T, Erdjument-Bromage, H, Cooper, MP, Ruas, JL, Chin, S, Tempst, P, Lazar, MA, Spiegelman, BM 2008. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes & Development 22, 13971409.CrossRefGoogle Scholar
Kassar-Duchossoy, L, Gayraud-Morel, B, Gomes, D, Rocancourt, D, Buckingham, M, Shinin, V, Tajbakhsh, S 2004. Mrf4 determines skeletal muscle identity in Myf5 : Myod double-mutant mice. Nature 431, 466471.CrossRefGoogle ScholarPubMed
Kazala, EC, Petrak, JL, Lozeman, FJ, Mir, PS, Laroche, A, Deng, J, Weselake, RJ 2003. Hormone-sensitive lipase activity in relation to fat content of muscle in Wagyu hybrid cattle. Livestock Production Science 79, 8796.CrossRefGoogle Scholar
Komatsu, T, Itoh, F, Hodate, K, Hazegawa, S, Obara, Y, Kushibiki, S 2005. Gene expression of resistin and Tnf-Alpha in adipose tissue of Japanese Black steers and Holstein steers. Animal Science Journal 76, 567573.CrossRefGoogle Scholar
Lafontan, M, Langin, D 2009. Lipolysis and lipid mobilization in human adipose tissue. Progress in Lipid Research 48, 275297.CrossRefGoogle ScholarPubMed
Lassar, AB, Davis, RL, Wright, WE, Kadesch, T, Murre, C, Voronova, A, Baltimore, D, Weintraub, H 1991. Functional-activity of myogenic Hlh proteins requires hetero-oligomerization with E12/E47-like proteins invivo. Cell 66, 305315.CrossRefGoogle Scholar
Lefterova, MI, Lazar, MA 2009. New developments in adipogenesis. Trends in Endocrinology and Metabolism 20, 107114.CrossRefGoogle ScholarPubMed
Lehnert, SA, Reverter, A, Byrne, KA, Wang, Y, Nattrass, GS, Hudson, NJ, Greenwood, PL 2007. Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Developmental Biology 7, 95.CrossRefGoogle ScholarPubMed
Lepper, C, Conway, SJ, Fan, CM 2009. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460, 627631.CrossRefGoogle ScholarPubMed
Lomax, MA, Sadiq, F, Karamanlidis, G, Karamitri, A, Trayhurn, P, Hazlerigg, DG 2007. Ontogenic loss of brown adipose tissue sensitivity to beta-adrenergic stimulation in the ovine. Endocrinology 148, 461468.CrossRefGoogle ScholarPubMed
Lulu Strat, A, Kokta, TA, Dodson, MV, Gertler, A, Wu, Z, Hill, RA 2005. Early signaling interactions between the insulin and leptin pathways in bovine myogenic cells. Biochimica et Biophysica Acta 1744, 164175.CrossRefGoogle ScholarPubMed
Maier, A, McEwan, JC, Dodds, KG, Fischman, DA, Fitzsimons, RB, Harris, AJ 1992. Myosin heavy-chain composition of single fibers and their origins and distribution in developing fascicles of sheep tibialis cranialis muscles. Journal of Muscle Research and Cell Motility 13, 551572.CrossRefGoogle ScholarPubMed
Martin, GS, Carstens, GE, Taylor, TL, Sweatt, CR, Eli, AG, Lunt, DK, Smith, SB 1997. Prepartum protein restriction does not alter norepinephrine-induced thermogenesis or brown adipose tissue function in newborn calves. Journal of Nutrition 127, 19291937.CrossRefGoogle ScholarPubMed
May, SG, Savell, JW, Lunt, DK, Wilson, JJ, Laurenz, JC, Smith, SB 1994. Evidence for preadipocyte proliferation during culture of subcutaneous and intramuscular adipose tissues from Angus and Wagyu crossbred steers. Journal of Animal Science 72, 31103117.CrossRefGoogle ScholarPubMed
McPherron, AC, Lawler, AM, Lee, S-J 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 8390.CrossRefGoogle ScholarPubMed
Miller, MF, Cross, HR, Lunt, DK, Smith, SB 1991. Lipogenesis in acute and 48-hour cultures of bovine intramuscular and subcutaneous adipose tissue explants. Journal of Animal Science 69, 162170.CrossRefGoogle ScholarPubMed
Muhlhausler, BS, Duffield, JA, Mcmillen, IC 2007. Increased maternal nutrition increases leptin expression in perirenal and subcutaneous adipose tissue in the postnatal lamb. Endocrinology 148, 61576163.CrossRefGoogle ScholarPubMed
Nakatani, M, Takehara, Y, Sugino, H, Matsumoto, M, Hashimoto, O, Hasegawa, Y, Murakami, T, Uezumi, A, Takeda, S, Noji, S, Sunada, Y, Tsuchida, K 2008. Transgenic expression of a myostatin inhibitor derived from follistatin increases skeletal muscle mass and ameliorates dystrophic pathology in mdx mice. FASEB Journal 22, 477487.CrossRefGoogle ScholarPubMed
Nedergaard, J, Bengtsson, T, Cannon, B 2007. Unexpected evidence for active brown adipose tissue in adult humans. American Journal of Physiology – Endocrinology and Metabolism 293, E444E452.CrossRefGoogle ScholarPubMed
Newby, D, Gertler, A, Vernon, RG 2001. Effects of recombinant ovine leptin on in vitro lipolysis and lipogenesis in subcutaneous adipose tissue from lactating and nonlactating sheep. Journal of Animal Science 79, 445452.CrossRefGoogle ScholarPubMed
Ohsaki, H, Sawa, T, Sasazaki, S, Kano, K, Taniguchi, M, Mukai, F, Mannen, H 2007. Stearoyl-Coa desaturase mRNA expression during bovine adipocyte differentiation in primary culture derived from japanese black and holstein cattle. Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 148, 629634.CrossRefGoogle ScholarPubMed
Ohyama, M, Matsuda, K, Torii, S, Matsui, T, Yano, H, Kawada, T, Ishihara, T 1998. The interaction between vitamin a and thiazolidinedione on bovine adipocyte differentiation in primary culture. Journal of Animal Science 76, 6165.CrossRefGoogle ScholarPubMed
Oustanina, S, Hause, G, Braun, T 2004. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO Journal 23, 34303439.CrossRefGoogle Scholar
Owens, FN, Gill, DR, Secrist, DS, Coleman, SW 1995. Review of some aspects of growth and development of feedlot cattle. Journal of Animal Science 73, 31523172.CrossRefGoogle ScholarPubMed
Palsson, H 1955. Conformation and body composition. In Progress in the physiology of farm animals (ed. J Hammond), pp. 430542. Butterworths, London, UK.Google Scholar
Pethick, DW, Barendse, W, Hocquette, JF, Thompson, JM, Wang, YH 2007. Regulation of marbling and body composition – growth and development, gene markers and nutritional biochemistry. In Energy and Protein Metabolism and Nutrition (ed. I Ortigues-Marty), pp. 7588. Wageningen Academic Publishers, Wageningen, The Netherlands.Google Scholar
Picard, B, Cassar-Malek, I 2009. Evidence for expression of IIb myosin heavy chain isoform in some skeletal muscles of Blonde d’Aquitaine bulls. Meat Science 82, 3036.CrossRefGoogle ScholarPubMed
Picard, B, Depreux, F, Geay, Y 1998. Muscle differentiation of normal and double-muscled bovine foetal myoblasts in primary culture. Basic Applied Myology 8, 197203.Google Scholar
Picard, B, Robelin, J, Pons, F, Geay, Y 1994. Comparison of the fetal development of fiber types in 4 Bovine muscles. Journal of Muscle Research and Cell Motility 15, 473486.CrossRefGoogle ScholarPubMed
Picard, B, Gagnière, H, Robelin, J, Geay, Y 1995. Comparison of the foetal development of muscle in normal and double-muscled cattle. Journal of Muscle Research and Cell Motility 16, 629639.CrossRefGoogle ScholarPubMed
Picard, B, Lefaucheur, L, Berri, C, Duclos, J-M 2002. Muscle fibre ontogenesis in farm animal species. Reproduction Nutrition Development 42, 415431.CrossRefGoogle ScholarPubMed
Picard, B, Jurie, C, Duris, MP, Renand, G 2006. Consequences of selection for higher growth rate on muscle fibre development in cattle. Livestock Science 102, 107120.CrossRefGoogle Scholar
Redmer, DA, Wallace, JM, Reynolds, LP 2004. Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development. Domestic Animal Endocrinology 27, 199217.CrossRefGoogle ScholarPubMed
Relaix, F, Montarras, D, Zaffran, S, Gayraud-Morel, B, Rocancourt, D, Tajbakhsh, S, Mansouri, A, Cumano, A, Buckingham, M 2006. Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. Journal of Cell Biology 172, 91102.CrossRefGoogle ScholarPubMed
Rhodes, SJ, Konieczny, SF 1989. Identification of Mrf4 – a new member of the muscle regulatory factor gene family. Genes & Development 3, 20502061.CrossRefGoogle ScholarPubMed
Robelin, J 1981. Cellularity of bovine adipose tissues – developmental-changes from 15-percent to 65-percent mature weight. Journal of Lipid Research 22, 452457.CrossRefGoogle Scholar
Robelin, J, Chilliard, Y 1989. Short-term and long-term effects of early nutritional deprivation on adipose tissue growth and metabolism in calves. Journal of Dairy Science 72, 505513.CrossRefGoogle ScholarPubMed
Robelin, J, Casteilla, L 1990. Differenciation, croissance et développement du tissu adipeux. Productions Animales 3, 243252.CrossRefGoogle Scholar
Robelin, J, Barboiron, C, Jailler, R 1985. Cellularité des différents dépôts adipeux des bovins en croissance. Reproduction Nutrition Development 25, 211214.CrossRefGoogle Scholar
Rudnicki, MA, Schnegelsberg, PNJ, Stead, RH, Braun, T, Arnold, HH, Jaenisch, R 1993. Myod or Myf-5 Is required for the formation of skeletal-muscle. Cell 75, 13511359.CrossRefGoogle ScholarPubMed
Russell, RG, Oteruelo, FT 1981. An ultrastructural-study of the differentiation of skeletal-muscle in the bovine fetus. Anatomy and Embryology 162, 403417.CrossRefGoogle ScholarPubMed
Schoonmaker, JP, Fluharty, FL, Loerch, SC 2004. Effect of source and amount of energy and rate of growth in the growing phase on adipocyte cellularity and lipogenic enzyme activity in the intramuscular and subcutaneous fat depots of Holstein steers. Journal of Animal Science 82, 137148.CrossRefGoogle ScholarPubMed
Seale, P, Kajimura, S, Spiegelman, BM 2009. Transcriptional control of brown adipocyte development and physiological function – of mice and men. Genes & Development 23, 788797.CrossRefGoogle ScholarPubMed
Seale, P, Sabourin, LA, Girgis-Gabardo, A, Mansouri, A, Gruss, P, Rudnicki, MA 2000. Pax7 is required for the specification of myogenic satellite cells. Cell 102, 777786.CrossRefGoogle ScholarPubMed
Seale, P, Kajimura, S, Yang, W, Chin, S, Rohas, LM, Uldry, M, Tavernier, G, Langin, D, Spiegelman, BM 2007. Transcriptional control of brown fat determination by PRDM16. Cell Metabolism 6, 3854.CrossRefGoogle ScholarPubMed
Seale, P, Bjork, B, Yang, W, Kajimura, S, Chin, S, Kuang, S, Scime, A, Devarakonda, S, Conroe, HM, Erdjument-Bromage, H, Tempst, P, Rudnicki, MA, Beier, DR, Spiegelman, BM 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961967.CrossRefGoogle Scholar
Shingu, H, Hodate, K, Kushibiki, S, Ueda, Y, Watanabe, A, Shinoda, M, Matsumoto, M 2001. Profiles of growth hormone and insulin secretion, and glucose response to insulin in growing Japanese Black heifers (beef type): comparison with Holstein heifers (dairy type). Comparative Biochemistry and Physiology – Toxicology and Pharmacology 130, 259270.CrossRefGoogle ScholarPubMed
Shrager, JB, Desjardins, PR, Burkman, JM, Konig, SK, Stewart, DR, Su, L, Shah, MC, Bricklin, E, Tewari, M, Hoffman, R, Rickels, MR, Jullian, EH, Rubinstein, NA, Stedman, HH 2000. Human skeletal myosin heavy chain genes are tightly linked in the order embryonic-IIa-IId/x-IIb-perinatal-extraocular. Journal of Muscle Research and Cell Motility 21, 345355.CrossRefGoogle Scholar
Smith, SB, Carstens, GE, Randel, RD, Mersmann, HJ, Lunt, DK 2004. Brown adipose tissue development and metabolism in ruminants. Journal of Animal Science 82, 942954.CrossRefGoogle ScholarPubMed
Soret, B, Lee, H, Finley, E, Lee, S, Vernon, R 1999. Regulation of differentiation of sheep subcutaneous and abdominal preadipocytes in culture. Journal of Endocrinology 161, 517524.CrossRefGoogle ScholarPubMed
Spalding, KL, Arner, E, Westermark, PO, Bernard, S, Buchholz, BA, Bergmann, O, Blomqvist, L, Hoffstedt, J, Naslund, E, Britton, T, Concha, H, Hassan, M, Ryden, M, Frisen, J, Arner, P 2008. Dynamics of fat cell turnover in humans. Nature 453, 783787.CrossRefGoogle ScholarPubMed
Sprinkle, JE, Ferrell, CL, Holloway, JW, Warrington, BG, Greene, LW, Wu, G, Stuth, JW 1998. Adipose tissue partitioning of limit-fed beef cattle and beef cattle with ad libitum access to feed differing in adaptation to heat. Journal of Animal Science 76, 665673.CrossRefGoogle ScholarPubMed
Sudre, K, Leroux, C, Pietu, G, Cassar-Malek, I, Petit, E, Listrat, A, Auffray, C, Picard, B, Martin, P, Hocquette, JF 2003. Transcriptome analysis of two bovine muscles during ontogenesis. Journal of Biochemistry (Tokyo) 133, 745756.CrossRefGoogle ScholarPubMed
Sumner, JM, Mcnamara, JP 2007. Expression of lipolytic genes in the adipose tissue of pregnant and lactating Holstein dairy cattle. Journal of Dairy Science 90, 52375246.CrossRefGoogle ScholarPubMed
Symonds, ME, Stephenson, T, Gardner, DS, Budge, H 2007. Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reproduction Fertility and Development 19, 5363.CrossRefGoogle ScholarPubMed
Tajbakhsh, S 2005. Skeletal muscle stem and progenitor cells: reconciling genetics and lineage. Experimental Cell Research 306, 364372.CrossRefGoogle ScholarPubMed
Tajbakhsh, S, Rocancourt, D, Cossu, G, Buckingham, M 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127138.CrossRefGoogle ScholarPubMed
Tan, SH, Reverter, A, Wang, Y, Byrne, KA, McWilliam, SM, Lehnert, SA 2006. Gene expression profiling of bovine in vitro adipogenesis using a cDNA microarray. Functional & Integrative Genomics 6, 235249.CrossRefGoogle ScholarPubMed
Tang, W, Zeve, D, Suh, JM, Bosnakovski, D, Kyba, M, Hammer, RE, Tallquist, MD, Graff, JM 2008. White fat progenitor cells reside in the adipose vasculature. Science 322, 583586.CrossRefGoogle ScholarPubMed
Taniguchi, M, Leluo, G, Bing, Z, Dodson, MV, Okine, E, Moore, SS 2008. Gene expression patterns of bovine perimuscular preadipocytes during adipogenesis. Biochemical and Biophysical Research Communications 366, 346351.CrossRefGoogle ScholarPubMed
Therkildsen, M 2005. Muscle protein degradation in bull calves with compensatory growth. Livestock Production Science 98, 205218.CrossRefGoogle Scholar
Timmons, JA, Wennmalm, K, Larsson, O, Walden, TB, Lassmann, T, Petrovic, N, Hamilton, DL, Gimeno, RE, Wahlestedt, C, Baar, K, Nedergaard, J, Cannon, B 2007. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proceedings of the National Academy of Sciences of the United States of America 104, 44014406.CrossRefGoogle Scholar
Torii, S, Ohyama, M, Matsui, T, Yano, H 1998. Ascorbic acid-2 phosphate enhances adipocyte differentiation of cultured stromal vascular cells prepared from bovine perirenal adipose tissue. Animal Science and Technology 69, 439444.Google Scholar
Tseng, YH, Kokkotou, E, Schulz, TJ, Huang, TL, Winnay, JN, Taniguchi, CM, Tran, TT, Suzuki, R, Espinoza, DO, Yamamoto, Y, Ahrens, MJ, Dudley, AT, Norris, AW, Kulkarni, RN, Kahn, CR 2008. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 10001004.CrossRefGoogle ScholarPubMed
Tudor, GD, Utting, DW, O’Rourke, PK 1980. The effect of pre- and post-natal nutrition on the growth of beef cattle. 3. The effect of severe restriction in early post-natal life on the development of the body components and chemical composition. Australian Journal of Agricultural Research 31, 191204.CrossRefGoogle Scholar
Tzahor, E 2009. Heart and craniofacial muscle development: a new developmental theme of distinct myogenic fields. Developmental Biology 327, 273279.CrossRefGoogle ScholarPubMed
Underwood, KR, Means, WJ, Zhu, MJ, Ford, SP, Hess, BW, Du, M 2008. AMP-activated protein kinase is negatively associated with intramuscular fat content in longissimus dorsi muscle of beef cattle. Meat Science 79, 394402.CrossRefGoogle ScholarPubMed
Valdez, MR, Richardson, JA, Klein, WH, Olson, EN 2000. Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Developmental Biology 219, 287298.CrossRefGoogle ScholarPubMed
Vernon, RG 1980. Lipid metabolism in the adipose tissue of ruminant animals. Progress in Lipid Research 19, 23106.CrossRefGoogle ScholarPubMed
Vernon, RG 1986. The growth and metabolism of adipocytes. In Control and Manipulation of Animal Growth (ed. PJ Buttery, NB Haynes and DB Lindsay), pp. 6783. Butterworths, London, UK.CrossRefGoogle Scholar
Wang, YH, Byrne, KA, Reverter, A, Harper, GS, Taniguchi, M, McWilliam, SM, Mannen, H, Oyama, K, Lehnert, SA 2005. Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mammalian Genome 16, 201210.CrossRefGoogle ScholarPubMed
Wegner, J, Albrecht, E, Fiedler, I, Teuscher, F, Papstein, HJ, Ender, K 2000. Growth- and breed-related changes of muscle fiber characteristics in cattle. Journal of Animal Science 78, 14851496.CrossRefGoogle ScholarPubMed
Wright, WE, Sassoon, DA, Lin, VK 1989. Myogenin, a factor regulating myogenesis, has a domain Homologous to Myod. Cell 56, 607617.CrossRefGoogle Scholar
Wu, G, Bazer, FW, Wallace, JM, Spencer, TE 2006. Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 23162337.CrossRefGoogle ScholarPubMed
Xu, CX, Oh, YK, Lee, HG, Kim, TG, Li, ZH, Yin, JL, Jin, YC, Jin, H, Kim, YJ, Kim, KH, Yeo, JM, Choi, YJ 2008. Effect of feeding high-temperature, microtime-treated diets with different lipid sources on conjugated linoleic acid formation in finishing Hanwoo steers. Journal of Animal Science 86, 30333044.CrossRefGoogle ScholarPubMed
Xu, JX, Albrecht, E, Viergutz, T, Nurnberg, G, Zhao, RQ, Wegner, J 2009. Perilipin, C/Ebpalpha, and C/Ebpbeta mrna abundance in longissimus muscle and different adipose tissues of Holstein and Charolais cattle. Meat Science 83, 120126.CrossRefGoogle Scholar
Xue, B, Rim, J-S, Hogan, JC, Coulter, AA, Koza, RA, Kozak, LP 2007. Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. Journal of Lipid Research 48, 4151.CrossRefGoogle ScholarPubMed
Yamada, T, Kawakami, SI, Nakanishi, N 2009. Expression of adipogenic transcription factors in adipose tissue of fattening Wagyu and Holstein steers. Meat Science 81, 8692.CrossRefGoogle ScholarPubMed
Zechner, R, Kienesberger, PC, Haemmerle, G, Zimmermann, R, Lass, A 2009. Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. Journal of Lipid Research 50, 321.CrossRefGoogle ScholarPubMed
Zembayashi, M 1994. Effects of nutritional planes and breeds on intramuscular-lipid deposition in M. longissimus dorsi of steers. Meat Science 38, 367374.CrossRefGoogle Scholar
Zhu, MJ, Ford, SP, Means, WJ, Hess, BW, Nathanielsz, PW, Du, M 2006. Maternal nutrient restriction affects properties of skeletal muscle in offspring. Journal of Physiology (London) 575, 241250.CrossRefGoogle ScholarPubMed
Zhu, MJ, Han, B, Tong, J, Ma, C, Kimzey, JM, Underwood, KR, Xiao, Y, Hess, B, Ford, SP, Nathanielsz, PW, Du, M 2008. Amp-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. Journal of Physiology (London) 586, 26512664.CrossRefGoogle ScholarPubMed