Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-08T16:29:38.625Z Has data issue: false hasContentIssue false
  • English
  • Français

Postnatal regulation of myosin heavy chain isoform expression and metabolic enzyme activity by nutrition

Published online by Cambridge University Press:  09 March 2007

P. White ,
D. Cattaneo  and
M. J. Dauncey
P. White
Affiliation:
The Babraham Institute, Cambridge CB2 4AT, UK
D. Cattaneo
Affiliation:
The Babraham Institute, Cambridge CB2 4AT, UK
M. J. Dauncey*
Affiliation:
The Babraham Institute, Cambridge CB2 4AT, UK
*
*Corresponding author: Dr M. J. Dauncey, fax +44 (0) 1223 496032, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Development of muscle is critically dependent on several hormones which in turn are regulated by nutritional status. We therefore determined the impact of mild postnatal undernutrition on key markers of myofibre function: type I slow myosin heavy chain (MyHC) isoform, myosin ATPase, succinate dehydrogenase and α-glycerophosphate dehydrogenase. In situ hybridization, immunocytochemistry and enzyme histochemistry were used to assess functionally distinct muscles from 6-week-old pigs which had been fed an optimal (6 % (60 g food/kg body weight per d)) or low (2 % (20 g food/kg per d)) intake for 3 weeks, and kept at 26°C. Nutritional status had striking muscle-specific influences on contractile and metabolic properties of myofibres, and especially on myosin isoform expression. A low food intake upregulated slow MyHC mRNA and protein levels in rhomboideus by 53 % (P < 0·01) and 18 % (P < 0·05) respectively; effects in longissimus dorsi, soleus and diaphragm were not significant. The oxidative capacity of all muscles increased on the low intake, albeit to varying extents: longissimus dorsi (55 %), rhomboideus (30 %), soleus (21 %), diaphragm (7 %). Proportions of slow oxidative fibres increased at the expense of fast glycolytic fibres. These novel findings suggest a critical role for postnatal nutrition in regulating myosin gene expression and muscle phenotype. They have important implications for optimal development of human infants: on a low intake, energetic efficiency will increase and the integrated response to many metabolic and growth hormones will alter, since both are dependent on myofibre type. Mechanisms underlying these changes probably involve complex interactions between hormones acting as nutritional signals and differential effects on their cell membrane receptors or nuclear receptors.

Keywords

Energy balanceMyosin heavy chain isoformsRespiratory enzymesSkeletal muscle developmentUndernutrition
Type
Research Article
Information
British Journal of Nutrition , Volume 84 , Issue 2 , August 2000 , pp. 185 - 194
Copyright
Copyright © The Nutrition Society 2000

References

Ayling, CM, Zanelli, JM, Moreland, BM and Schulster, D (1992) Effect of human growth hormone injection on the fibre type composition and metabolic activity in a skeletal muscle from normal and hypophysectomized rats. Growth Regulation 2, 133–143.Google Scholar
Barker, DJ (1995) The Wellcome Foundation Lecture, 1994. The fetal origins of adult disease. Proceedings of the Royal Society of London. Series B: Biological Sciences 262, 37–43.Google ScholarPubMed
Brozanski, BS, Daood, MJ, LaFramboise, WA, Watchko, JF, Foley, TP Jr, Butler-Browne, GS, Whalen, RG, Guthrie, RD and Ontell, M (1991) Effects of perinatal undernutrition on elimination of immature myosin isoforms in the rat diaphragm. American Journal of Physiology 261, L49–L54.Google ScholarPubMed
Bruhat, A, Jousse, C and Fafournoux, P (1999) Amino acid limitation regulates gene expression. Proceedings of the Nutrition Society 58, 625–632.CrossRefGoogle ScholarPubMed
Chang, KC, Fernandes, K and Goldspink, G (1993) In vivo expression and molecular characterization of the porcine slow-myosin heavy chain. Journal of Cell Science 106, 331–341.CrossRefGoogle ScholarPubMed
Cotter, MA and Cameron, NE (1994) Metabolic, neural and vascular influences on muscle function in experimental models of diabetes mellitus and related pathological states. Basic and Applied Myology 4, 293–307.Google Scholar
d'Albis, A and Butler-Browne, G (1993) The hormonal control of myosin isoform expression in skeletal muscle of mammals: a review. Basic and Applied Myology 3, 7–16.Google Scholar
Dauncey, MJ (1997) From early nutrition and later development. to underlying mechanisms and optimal health. British Journal of Nutrition 78(Suppl. 2), S113–S123.CrossRefGoogle ScholarPubMed
Dauncey, MJ, Burton, KA, White, P, Harrison, AP, Gilmour, RS, Duchamp, C and Cattaneo, D (1994) Nutritional regulation of growth hormone receptor gene expression. FASEB Journal 8, 81–88.CrossRefGoogle ScholarPubMed
Dauncey, MJ and Gilmour, RS (1996) Regulatory factors in the control of muscle development. Proceedings of the Nutrition Society 55, 543–559.CrossRefGoogle ScholarPubMed
Dauncey, MJ, Holder, G, Ingram, DL, Rudd, BT and Shakespear, RA (1989) Thermal and nutritional regulation of insulin-like growth factor-I and cortisol in the young pig. Journal of Physiology (London) 418, 175P.Google Scholar
Dauncey, MJ and Ingram, DL (1988) Influence of environmental temperature and energy intake on skeletal muscle respiratory enzymes and morphology. European Journal of Applied Physiology and Occupational Physiology 58, 239–244.CrossRefGoogle ScholarPubMed
Duchamp, C, Burton, KA, Herpin, P and Dauncey, MJ (1996) Perinatal ontogeny of porcine growth hormone receptor gene expression is modulated by thyroid status. European Journal of Endocrinology 134, 524–531.CrossRefGoogle ScholarPubMed
Ferré, P (1999) Regulation of gene expression by glucose. Proceedings of the Nutrition Society 58, 621–623.CrossRefGoogle ScholarPubMed
Florini, JR and Ewton, DZ (1992) Induction of gene expression in muscle by the IGFs. Growth Regulation 2, 23–29.Google ScholarPubMed
Girard, J, Perdereau, D, Foufelle, F, Prip-Buus, C and Ferré, P (1994) Regulation of lipogenic enzyme gene expression by nutrients and hormones. FASEB Journal 8, 36–42.CrossRefGoogle ScholarPubMed
Goldspink, G (1996) Muscle growth and muscle function: a molecular biological perspective. Research in Veterinary Science 60, 193–204.CrossRefGoogle ScholarPubMed
Goldspink, G, Scutt, A, Loughna, PT, Wells, DJ, Jaenicke, T and Gerlach, GF (1992) Gene expression in skeletal muscle in response to stretch and force generation. American Journal of Physiology 262, R356–363.Google ScholarPubMed
Harridge, SDR, Bottinelli, R, Canepari, M, Pellegrino, MA, Reggiani, C, Esbjornsson, M and Saltin, B (1996) Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflügers Archiv (European Journal of Physiology) 432, 913–920.CrossRefGoogle ScholarPubMed
Harrison, AP, Latorre, R and Dauncey, MJ (1997) Postnatal development and differentiation of myofibres in functionally diverse porcine skeletal muscles. Reproduction, Fertility, and Development 9, 731–740.CrossRefGoogle ScholarPubMed
Harrison, AP, Rowlerson, AM and Dauncey, MJ (1996) Selective regulation of myofiber differentiation by energy status during postnatal development. American Journal of Physiology 270, R667–674.Google ScholarPubMed
Harrison, AP, Tivey, DR, Clausen, T, Duchamp, C and Dauncey, MJ (1996) Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutrition. British Journal of Nutrition 76, 841–855.CrossRefGoogle ScholarPubMed
Henriksson, J (1990) The possible role of skeletal muscle in the adaptation to periods of energy deficiency. European Journal of Clinical Nutrition 44, 55–64.Google ScholarPubMed
Herpin, P, Berthon, D, Duchamp, C, Dauncey, MJ and Le Dividich, J (1996) Effect of thyroid status in the perinatal period on oxidative capacities and mitochondrial respiration in porcine liver and skeletal muscle. Reproduction, Fertility and Development 8, 147–155.CrossRefGoogle ScholarPubMed
Herpin, P and Lefaucheur, L (1992) Adaptative changes in oxidative metabolism in skeletal muscle of cold acclimated piglets. Journal of Thermal Biology 17, 277–285.CrossRefGoogle Scholar
Hoet, JJ and Hanson, MA (1999) Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. Journal of Physiology (London) 514, 617–627.CrossRefGoogle ScholarPubMed
Katsumata, M, Burton, KA, Li, J and Dauncey, MJ (1999) Suboptimal energy balance selectively up-regulates muscle GLUT gene expression but reduces insulin-dependent glucose uptake during postnatal development. FASEB Journal 13, 1405–1413.CrossRefGoogle ScholarPubMed
Katsumata, M, Burton, KA, White, P, Cattaneo, D and Dauncy, MJ (1997) Growth hormone receptor gene expression is related to metabolic and contractile properties of muscle. Journal of Endocrinology 152, P125.Google Scholar
Lefaucheur, L, Edom, F, Ecolan, P and Butler-Browne, GS (1995) Pattern of muscle fiber type formation in the pig. Developmental Dynamics 203, 27–41.CrossRefGoogle ScholarPubMed
Lefaucheur, L, Hoffman, RK, Gerrard, DE, Okamura, CS, Rubinstein, N and Kelly, A (1998) Evidence for three adult fast myosin heavy chain isoforms in type II skeletal muscle fibers in pigs. Journal of Animal Science 76, 1584–1593.CrossRefGoogle ScholarPubMed
Li, J, Owens, JA, Owens, PC, Saunders, JC, Fowden, AL and Gilmour, RS (1996) The ontogeny of hepatic growth hormone receptor and insulin-like growth factor I gene expression in the sheep fetus during late gestation: developmental regulation by cortisol. Endocrinology 137, 1650–1657.CrossRefGoogle ScholarPubMed
Lucas, A (1994) Role of nutritional programming in determining adult morbidity. Archives of Disease in Childhood 71, 288–290.CrossRefGoogle ScholarPubMed
Mascarello, F, Stecchini, ML, Rowlerson, A and Ballocchi, E (1992) Tertiary myotubes in postnatal growing pig muscle detected by their myosin isoform composition. Journal of Animal Science 70, 1806–1813.CrossRefGoogle ScholarPubMed
McKoy, G, Leger, ME, Bacou, F and Goldspink, G (1998) Differential expression of myosin heavy chain mRNA and protein isoforms in four functionally diverse rabbit skeletal muscles during pre- and postnatal development. Developmental Dynamics 211, 193–203.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Morovat, A and Dauncey, MJ (1998) Effects of thyroid status on insulin-like growth factor-I, growth hormone and insulin are modified by food intake. European Journal of Endocrinology 138, 95–103.CrossRefGoogle ScholarPubMed
Polla, B, Bottinelli, R, Sandoli, D, Sardi, C and Reggiani, C (1994) Cortisone-induced changes in myosin heavy chain distribution in respiratory and hindlimb muscles. Acta Physiologica Scandinavica 151, 353–361.CrossRefGoogle ScholarPubMed
Rowlerson, A (1994) An outline of fibre types in vertebrate skeletal muscle: histochemical identification and myosin isoforms. Basic and Applied Myology 4, 333–352.Google Scholar
Samec, S, Seydoux, J and Dulloo, AG (1998) Role of UCP homologues in skeletal muscles and brown adipose tissue: mediators of thermogenesis or regulators of lipids as fuel substrate?. FASEB Journal 12, 715–724.CrossRefGoogle ScholarPubMed
Schantz, P, Henriksson, J and Jansson, E (1983) Adaptation of human skeletal muscle to endurance training of long duration. Clinical Physiology 3, 141–151.CrossRefGoogle ScholarPubMed
Schiaffino, S and Reggiani, C (1994) Myosin isoforms in mammalian skeletal muscle. Journal of Applied Physiology 77, 493–501.CrossRefGoogle ScholarPubMed
Stickland, NC, Widdowson, EM and Goldspink, G (1975) Effects of severe energy and protein deficiencies on the fibres and nuclei in skeletal muscle of pigs. British Journal of Nutrition 34, 421–428.CrossRefGoogle ScholarPubMed
Swoap, SJ, Haddad, F, Caiozzo, VJ, Herrick, RE, McCue, SA and Baldwin, KM (1994) Interaction of thyroid hormone and functional overload on skeletal muscle isomyosin expression. Journal of Applied Physiology 77, 621–629.CrossRefGoogle ScholarPubMed
Tumbleson, ME & Schook, LB (1996) Advances in Swine in Biomedical Research. New York, NY: Plenum Press.CrossRefGoogle Scholar
Ward, SS and Stickland, NC (1993) The effect of undernutrition in the early postnatal period on skeletal muscle tissue. British Journal of Nutrition 69, 141–150.CrossRefGoogle ScholarPubMed
White, P and Dauncey, MJ (1999) Differential expression of thyroid hormone receptor isoforms is strikingly related to cardiac and skeletal muscle phenotype during postnatal development. Journal of Molecular Endocrinology 23, 241–254.CrossRefGoogle ScholarPubMed
Widdowson, EM and McCance RA (1975) A review: new thoughts on growth. Pediatric Research 9, 154–156.CrossRefGoogle ScholarPubMed