Abstract
Stimuli during pregnancy, such as protein restriction, can affect morphophysiological parameters in the offspring with consequences in adulthood. The phenomenon known as fetal programming can cause short- and long-term changes in the skeletal muscle phenotype. We investigated the morphology and the myogenic regulatory factors (MRFs) MyoD and myogenin expression in soleus, SOL; oxidative and slow twitching and in extensor digitorum longus, EDL; glycolytic and fast twitching muscles in the offspring of dams subjected to protein restriction during pregnancy. Four groups of male Wistar offspring rats were studied. Offspring from dams fed a low-protein diet (6 % protein, LP) and normal protein diet (17 % protein, NP) were euthanized at 30 and 112 days old, and their muscles were removed and kept at −80 °C. Muscles histological sections (8 μm) were submitted to a myofibrillar adenosine triphosphatase histochemistry reaction for morphometric analysis. Gene and protein expression levels of MyoD and myogenin were determined by RT-qPCR and western blotting. The major findings observed were distinct patterns of morphological changes in SOL and EDL muscles in LP offspring at 30 and 112 days old without changes in MRFs MyoD and myogenin expression. Our results indicate that maternal protein restriction followed by normal diet after birth induced morphological changes in muscles with distinct morphofunctional characteristics over the long term, but did not alter the MRFs MyoD and myogenin expression. Further studies are necessary to better understand the mechanisms underlying the maternal protein restriction response on skeletal muscle.
Similar content being viewed by others
References
Allen DL, Sartorius CA, Sycuro LK, Leinwand LA (2001) Different pathways regulate expression of the skeletal myosin heavy chain genes. J Biol Chem 276:43524–43533. doi:10.1074/jbc.M108017200
Always SE, Degens H, Krishnamurthy G, Smith CA (2002) Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Phys-Cell Physiol 283:C66–C76. doi:10.1152/ajpcell.00598.2001
Barker DJ (1994) Programming the baby. In: Barker DJ (ed) Mothers, babies, and disease in later life. BMJ Publishing Group, London, pp 14–36
Bayol S, Jones D, Goldspink G, Stickland NC (2004) The influence of undernutrition during gestation on skeletal muscle cellularity and on the expression of genes that control muscle growth. Br J Nutr 91:331–339. doi:10.1079/BJN20031070
Bedy KS, Birzgalis AR, Mahon M, Smart JL, Wareham AC (1982) Early life undernutrition in rats. Quantitative histology of skeletal muscles form underfed young and refed adult animal. Br J Nutr 47:417–431. doi:10.1079/BJN19820053
Beermann DH (1983) Effects of maternal dietary restriction during gestation and lactation, muscle, sex and age on various indices of skeletal muscle growth in the rat. J Anim Sci 57:328–337
Cullen MF, Johnsom MA, Mastaglia FL (1992) Pathological reactions of skeletal muscle. In: Mastaglia FL (ed) Skeletal muscle pathology, 2nd edn. Churchill Livingstone, New York, Tokio, pp 123–184
Daniel CTR, Brameld JM, Craigon J, Scollan D (2007) Effect of maternal dietary restriction during pregnancy on lamb carcass characteristics and muscle fiber composition Z. J Anim Sci 85:1565–1576. doi:10.2527/jas.2006-743
Daugaar JR, Nielsen JN, Kristiansen S, Andersen JL, Hargreaves M, Richte EA (2000) Fiber type–Specific expression of GLUT4 in human skeletal muscle Influence of exercise training. Diabetes 49(7):1092–1095. doi:10.2337/diabetes.49.7.1092
Davis TA, Fiorotto ML, Nguyen HV, Reeds PJ (1989) Protein turnover in skeletal muscle of suckling rats. Am J Physiol Regul Integr Comp Physiol 257:R1141–R1146
Dow DE, Cederna PS, Hasset CA, Kostrominova TY, Faulkner JA (2004) Number of contractions to maintain mass and force of a denervated rat muscle. Muscle Nerv 30(1):77–86. doi:10.1002/mus.20054
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. J Anim Sci 83:2564–2571
Fluck M, Hoppeler H (2003) Molecular basis of skeletal muscle plasticity-from gene to form and function. Rev Physiol Biochem Pharmacol 146:160–161. doi:10.1007/s10254-002-0004-7
Fowden AL, Giussani DA, Forhead AJ (2006) Intrauterine programming of physiological systems: causes and consequences. Physiology 21:29–37. doi:10.1152/physiol.00050.2005
Halseth AE, Bracy DP, Wasserman DH (2001) Functional limitations to glucose uptake in muscles comprised of different fiber types. Am J Physiol Endocrinol Metab 280:994–999
Huber K, Mile JL, Norman AM, Thompson NM, Davison M, Breier BH (2009) Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrin 150(9):4135–4144. doi:10.1210/en.2009-0125
Hughes SM, Taylor JM, Tapscott SJ, Gurley CM, Carter WJ, Peterson CA (1993) Selective accumulation of MyoD and myogenin mRNAs in fast and slow muscle is controlled by innervation and hormones. Development 118:1137–1147
Jackman RW, Kandarian SC (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287:834–843. doi:10.1152/ajpcell.00579.2003
Jensen CB, Storgaard H, Madsbad S, Richter EA, Vaag AA (2007) Altered skeletal muscle fiber composition and size precede whole-body insulin resistance in young men with low birth weight. J Clin Endocrinol Metab 92:1530–1534. doi:10.1210/jc.2006-2360
Johnston BY (1985) Sustained force development: specializations and variation among the vertebrates. J Exp Biol 115:239–251
Kelly AM; Rubinstein NA (2003) The diversity of muscle fiber types and its origin during development. In: Engel A (ed) Myology, 3rd edn. McGraw-Hill, pp 87:103
Kevin D, Sinclair R (2007) Modelling the developmental origins of health and disease in the early embryo Singh. Theriogenology 67:43–53. doi:10.1016/j.theriogenology.2006.09.017
Kronnie GT, Reggian C (2002) Skeletal muscle fibre type specification during embryonic development. J Muscle Res Cell Motil 23:65–69. doi:10.1023/A:1019940932275
Langley-Evans SC (2004) Fetal programming of adult disease: an overview. In: Langley-Evans SC (ed) Fetal Nutrition and Adult Disease Programming of Chronic Disease Through Fetal Exposure to Undernutrition, 8th edn. CABI, Wallingford, pp 1–20
Lin H, Yutzey HK, Konieczny SF (1991) Muscle-specific expression of the Troponin I gene requires interactions between Helix-Loop-Helix Muscle regulatory actors and Ubiquitous Transcription factors. Mol Cell Biol 11:267–280. doi:0270-7306/91/010267-14$02.00/0
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Loughna PT, Brownson C (1996) Two myogenic regulatory factor transcripts exhibit muscle-specific responses to disuse and passive stretch in adult rats. FEBS Lett 390:304–306. doi:10.1016/0014-5793(96)00681-3
Lucas A (1991) Programming in early nutrition in man. Ciba Foun Symp 156:38–53. doi:10.1002/9780470514047.ch4
Magaudda L, Mauro DD, Trimarchi F, Anastasi G (2004) Effects of physical exercises on skeletal muscle fiber: ultrastructural and molecular aspects. Basic Appl myol 14(1):17–21
Mallinson JE, Sculley DV, Craigon J, Plant R, Langley-Evans SC, Brameld JM (2007) Fetal exposure to a maternal low-protein diet during mid-gestation results in muscle-specific effects on fibre type composition in young rats. Br J Nutri 98:292–299. doi:10.1017/S0007114507701678
Megeney LA, Neufer PD, Dohm GL, Tan MH, Blewett CA, Elder GCB (1993) Effects of muscle activity and fiber composition on glucose transport and GLUT-4. Am J Physiol Endocrinol Metab 264(4):E583–E593
Mesquita J, Gontijo AR, Boer PA (2010) Maternal undernutrition and the offspring kidney: from fetal to adult Life. Braz J Med Biol Res 43(11):1010–1018. doi:10.1590/S0100-879X2010007500113
Murre C, Mccaw PS, Vaessin H (1989) Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537–544. doi:10.1016/0092-8674(89)90434-0
Ozanne SE, Olsen GS, Hansen LL, Tingey KJ, Nave BT, Wang CL (2003) Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol 177:235–241. doi:10.1677/joe.0.1770235
Parker MH, Seale P, Rudnicki M (2003) A. Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet 4:497–507. doi:10.1038/nrg1109
Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50:500–509. doi:10.1002/1097-029(20000915)50:6<500:AID-JEMT7>3.0.CO;2-7
Phillips DW, Barker DJP, Hales CN, First S, Osmond C (1994) Thinness at birth and insulin resistance. Diabetologia 37:150–154. doi:10.1007/s001250050086
Psilander N, Damsgaard R, Pilegaard H (2003) Resistance exercise alters MRF and IGF-I mRN content in human skeletal muscle. J Appl Physiol 95:1038–1044
Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 Purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76 rodent diet. J Nut 123:1939–1951
Sanchez H, Chapot R, Banzet S, Koulmann N, Birot O, Bigard AX, Peinnequin A (2006) Quantification by real-time PCR of developmental and adult myosin mRNA in rat muscles. Biochem biophys resh commun 340:165–174. doi:10.1016/j.bbrc.2005.11.172
Sandri M (2008) Signaling in muscle atrophy and hypertrophy. Physiology 23:160–170. doi:10.1152/physiol.00041.2007
Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos GER (1999) Fiber type composition of four hindlimb muscles of adult fisher 344 rats. Histochem Cell Biol 111:117–123. doi:10.1007/s004180050341
Toscano AE, Castro R, Canon F (2008) Effect of a low-protein diet during pregnancy on skeletal muscle mechanical properties of offspring rats. Nutrition: 24(3):270–278. doi:10.1016/j.nut.2007.12.004
Vandesompele J, Preter DE, Pattyn F, Poppe B, Van Roy N, Paepe A, Speleman F(2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 18:research0034.1-research0034.11. doi:10.1186/gb-2002-3-7-research0034
Voytik SL, Przyborski M, Badylak SF, Konieczny SF (1993) Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscle. Dev Dyn 198:214–224. doi:10.1002/aja.1001980307
Walters EH, Stickland NC, Loughna PT (2000) The expression of the myogenic regulatory factors in denervated and normal muscles of different phenotypes. J Muscle Res Cell Motil 21(7):647–653. doi:10.1023/A:100568382596
Wilson SJ, Ross JJ, Harris AJ (1988) A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development 102:815–821
Zar JH (2009) Biostatistical analysis. Pretice-Hole, New Jersey
Zhu MJ, Ford SP, Nathanielsz PW, Du M (2004) Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol Reprod 71:1968–1973. doi:10.1095/biolreprod.104.034561
Zhu MJ, Ford SP, Warrie J, Means WJ, Hess BW, Nathanielszand PW, Du M (2006) Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 15:241–250. doi:10.1113/jphysiol.2006.112110
Acknowledgments
This study was supported by FAPESP (Process no. 2007/59970-8) and FUNDUNESP (Process no. 00946/09-DFP). This work is part of a doctoral thesis that was presented by L.C.C. to São Paulo State University (UNESP) in 2011.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cabeço, L.C., Budri, P.E., Baroni, M. et al. Maternal protein restriction induce skeletal muscle changes without altering the MRFs MyoD and myogenin expression in offspring. J Mol Hist 43, 461–471 (2012). https://doi.org/10.1007/s10735-012-9413-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10735-012-9413-3