European Journal of Nutrition

, Volume 52, Issue 3, pp 1201–1213 | Cite as

Enhanced sensitivity of skeletal muscle growth in offspring of mice long-term selected for high body mass in response to a maternal high-protein/low-carbohydrate diet during lactation

  • Charlotte Rehfeldt
  • Martina Langhammer
  • Marzena Kucia
  • Gerd Nürnberg
  • Cornelia C. Metges
Original Contribution

Abstract

Aim

To investigate the effects of a high-protein/low-carbohydrate diet fed to mice of different genotypes during pregnancy and/or lactation on offspring skeletal muscle growth and metabolism.

Methods

Pregnant mice from strains selected for high body mass (DU6) or endurance running performance (DUhLB) and from an unselected control strain (DUK) were fed iso-energetic diets containing 20 % (C) or 40 % protein and low carbohydrate (HP) from mating to weaning at day 21 of age. At birth, offspring were cross-fostered resulting in different exposure to maternal prenatal-preweaning diets (C–C, HP–C, C–HP, HP–HP). Rectus femoris muscle of male mice (n = 291) was examined at day 23, 44, 181 and 396 of age for cellular growth and metabolism.

Results

At day 23 of age, body and muscle growth was retarded by 30–40 % (P < 0.0001) in response to the C–HP and HP–HP, but not to the HP–C diet, due to reduced fibre size (P < 0.0001) but not fibre number. DNA was highly reduced in DU6, less in DUhLB, but not in DUK muscle (strain × diet; P < 0.0001). Despite some compensation, muscle growth was still impaired (P < 0.001) in adulthood (day 44; day 181), but at senescence only in DU6 mice (strain × diet; P < 0.05). Only at weaning, isocitrate and lactate dehydrogenase activities were increased or decreased (P < 0.0001), respectively, without influence on fibre type composition.

Conclusion

A high-protein/low-carbohydrate diet fed to dams during lactation, but not during pregnancy, retards skeletal muscle growth in offspring with greater response of a heavy, obese compared with a physically fit and a control genotype and causes a transient shift towards oxidative versus glycolytic muscle metabolism.

Keywords

Genetic selection Protein/carbohydrate intake Pregnancy Lactation Genotype–nutrition interaction Muscle metabolism 

Notes

Acknowledgments

We thank Karin Zorn, Angela Steinborn, Marie-Jugert Lund, Monika Günther, and Ilka Genke for assistance with animal care, sample collection and laboratory analyses. This work was supported by the Commission of the European Community, within the FP 6 priority 5.4.3.1 Food quality and safety (EARNEST, Food-CT-2005-007036). It does not necessarily reflect the views of the Commission and in no way anticipates its future policy in this area.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

394_2012_431_MOESM1_ESM.pdf (179 kb)
Supplementary material 1 (PDF 179kb)

References

  1. 1.
    Battista MC, Hivert MF, Duval K, Baillargeon JP (2011) Intergenerational cycle of obesity and diabetes: how can we reduce the burdens of these conditions on the health of future generations? Exp Diabetes Res 2011:596060CrossRefGoogle Scholar
  2. 2.
    Tanentsapf I, Heitmann BL, Adegboye AR (2011) Systematic review of clinical trials on dietary interventions to prevent excessive weight gain during pregnancy among normal weight, overweight and obese women. BMC Pregnancy Childbirth 11:81CrossRefGoogle Scholar
  3. 3.
    Johnston CS, Day CS, Swan PD (2002) Postprandial thermogenesis is increased 100 % on a high-protein, low-fat diet versus a high-carbohydrate, low-fat diet in healthy, young women. J Am Coll Nutr 21:55–61Google Scholar
  4. 4.
    Halton TL, Hu FB (2004) The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr 23:373–385Google Scholar
  5. 5.
    Noakes M, Keogh JB, Foster PR, Clifton PM (2005) Effect of an energy-restricted, high-protein, low-fat diet relative to a conventional high-carbohydrate, low-fat diet on weight loss, body composition, nutritional status, and markers of cardiovascular health in obese women. Am J Clin Nutr 81:1298–1306Google Scholar
  6. 6.
    Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359:61–73CrossRefGoogle Scholar
  7. 7.
    Daenzer M, Ortmann S, Klaus S, Metges CC (2002) Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. J Nutr 132:142–144Google Scholar
  8. 8.
    Kucia M, Langhammer M, Gors S, Albrecht E, Hammon HM, Nurnberg G, Metges CC (2011) High-protein diet during gestation and lactation affects mammary gland mRNA abundance, milk composition and pre-weaning litter growth in mice. Animal 5:268–277CrossRefGoogle Scholar
  9. 9.
    Rehfeldt C, Lefaucheur L, Block J, Stabenow B, Pfuhl R, Otten W, Metges CC, Kalbe C (2012) Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. Eur J Nutr 51:151–165CrossRefGoogle Scholar
  10. 10.
    Campbell-Brown M, Johnstone FD, Kerr-Grieve JF (1986) The effect on birthweight of a high-protein, low carbohydrate diet during pregnancy. Proc Nutr Soc 45:90AGoogle Scholar
  11. 11.
    Andreasyan K, Ponsonby AL, Dwyer T, Morley R, Riley M, Dear K, Cochrane J (2007) Higher maternal dietary protein intake in late pregnancy is associated with a lower infant ponderal index at birth. Eur J Clin Nutr 61:498–508Google Scholar
  12. 12.
    Langhammer M, Derno M, Dietrich N, Renne U, Nurnberg G, Henning U, Metges CC (2006) Fetal programming of offspring growth due to maternal high protein diet is genotype dependent in mice. J Anim Sci 84(Suppl 1):184–191Google Scholar
  13. 13.
    Walther T, Dietrich N, Langhammer M, Kucia M, Hammon H, Renne U, Siems WE, Metges CC (2011) High-protein diet in lactation leads to a sudden infant death-like syndrome in mice. PLoS ONE 6:e17443CrossRefGoogle Scholar
  14. 14.
    Sayer AA, Stewart C, Patel H, Cooper C (2010) The developmental origins of sarcopenia: from epidemiological evidence to underlying mechanisms. JDOHaD 1:150–157Google Scholar
  15. 15.
    Bonen A (2010) Muscles as molecular and metabolic machines. Am J Physiol Endocrinol Metab 299:E143–E144Google Scholar
  16. 16.
    Rehfeldt C, Kuhn G (2006) Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. J Anim Sci 84(Suppl):E113–E123Google Scholar
  17. 17.
    Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B (2006) Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. J Anim Sci 84:93–103Google Scholar
  18. 18.
    Rehfeldt C, Stabenow B, Pfuhl R, Block J, Nurnberg G, Otten W, Metges CC, Kalbe C (2012) Effects of limited and excess protein intakes of pregnant gilts on carcass quality and cellular properties of skeletal muscle and subcutaneous adipose tissue in fattening pigs. J Anim Sci 90:184–196CrossRefGoogle Scholar
  19. 19.
    Gluckman PD, Hanson MA, Buklijas T (2010) A conceptual framework for the developmental origins of health and disease. JDOHaD 1:6–18Google Scholar
  20. 20.
    Thyfault JP, Booth FW (2011) Lack of regular physical exercise or too much inactivity. Curr Opin Clin Nutr Metab Care 14:374–378CrossRefGoogle Scholar
  21. 21.
    Johnstone AM, Horgan GW, Murison SD, Bremner DM, Lobley GE (2008) Effects of a high-protein ketogenic diet on hunger, appetite, and weight loss in obese men feeding ad libitum. Am J Clin Nutr 87:44–55Google Scholar
  22. 22.
    Metges CC, Lang IS, Hennig U, Brüssow K-P, Kanitz E, Tuchscherer M, Schneider F, Weitzel J, Ooster A, Sauerwein H, Bellmann O, Nürnberg G, Rehfeldt C, Otten W (2012) Intrauterine growth retarded progeny of pregnant sows fed high protein:low carbohydrate diet is related to metabolic energy deficit. PLoS ONE 7:e31390CrossRefGoogle Scholar
  23. 23.
    Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM (2003) Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. Am J Clin Nutr 78:31–39Google Scholar
  24. 24.
    Layman DK, Boileau RA, Erickson DJ, Painter JE, Shiue H, Sather C, Christou DD (2003) A reduced ratio of dietary carbohydrate to protein improves body composition and blood lipid profiles during weight loss in adult women. J Nutr 133:411–441Google Scholar
  25. 25.
    Devkota S, Layman DK (2010) Protein metabolic roles in treatment of obesity. Curr Opin Clin Nutr Metab Care 13:403–407CrossRefGoogle Scholar
  26. 26.
    Renne U, Dietl G, Langhammer M, Rehfeldt C, Nurnberg K, Kuhla S, Bünger L (2006) Phenotypic characterisation of extreme growth-selected mouse lines: an important prerequisite for future QTL analysis. CEJB 1:345–375Google Scholar
  27. 27.
    Falkenberg H, Renne U, Langhammer M (2000) Comparison of biochemical blood traits after long-term selection on high or low locomotory activity in mice. Arch Tierz-Arch Anim Breed 43:513–522Google Scholar
  28. 28.
    Walz C, Faustmann I, Renne U, Ponsuksili S, Kehr J, Fiehn O, Schwerin M (2005) Long-term endurance fitness selected mice exhibit extended changes of expression patterns in muscle, liver and heart compared to unselected mice. FEBS J 272(Suppl S1): 448Google Scholar
  29. 29.
    Schüler L (1985) Der Mäuseauszuchtstamm Fzt:DU und seine Anwendung als Modell in der Tierzuchtforschung [Mouse strain Fzt:DU and its use as model in animal breeding research]. Arch Tierz-Arch Anim Breed 28:357–362Google Scholar
  30. 30.
    Bünger L, Laidlaw A, Bulfield G, Eisen EJ, Medrano JF, Bradford GE, Pirchner F, Renne U, Schlote W, Hill WG (2001) Inbred lines of mice derived from long-term growth selected lines: unique resources for mapping growth genes. Mamm Genome 12:678–686CrossRefGoogle Scholar
  31. 31.
    Renne U, Langhammer M, Wytrwat E, Dietl G, Bünger L (2003) Genetic-statistical analysis of growth in selected and unselected mouse lines. J Exp Anim Sci 42:218–232CrossRefGoogle Scholar
  32. 32.
    Rehfeldt C, Walther K (1997) A combined assay for DNA, protein, and incorporated [3H] label in cultured muscle cells. Anal Biochem 251:294–297CrossRefGoogle Scholar
  33. 33.
    Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356CrossRefGoogle Scholar
  34. 34.
    Huber K, Petzold J, Rehfeldt C, Ender K, Fiedler I (2007) Muscle energy metabolism: structural and functional features in different types of porcine striated muscles. J Muscle Res Cell Motil 28:249–258CrossRefGoogle Scholar
  35. 35.
    Rehfeldt C, Ott G, Gerrard DE, Varga L, Schlote W, Williams JL, Renne U, Bunger L (2005) Effects of the Compact mutant myostatin allele Mstn (Cmpt-dl1Abc) introgressed into a high growth mouse line on skeletal muscle cellularity. J Muscle Res Cell Motil 26:103–112CrossRefGoogle Scholar
  36. 36.
    Rehfeldt C, Renne U, Sawitzky M, Binder G, Hoeflich A (2010) Increased fat mass, decreased myofiber size, and a shift to glycolytic muscle metabolism in adolescent male transgenic mice overexpressing IGFBP-2. Am J Physiol Endocrinol Metab 299:E287–E298Google Scholar
  37. 37.
    Schadereit R, Rehfeldt C, Krawielitzki K, Klein K, Kanitz E, Kuhla S (1998) Protein turnover, body composition, muscle characteristics, and blood hormones in response to different direction of growth selection in mice. J Anim Feed Sci 7:333–352Google Scholar
  38. 38.
    Mitchell RD, Burke WH (1995) Posthatching growth and pectoralis muscle development in broiler strain chickens, bantam chickens and the reciprocal crosses between them. Growth Dev Aging 59:149–161Google Scholar
  39. 39.
    Rehfeldt C, Walther K, Albrecht E, Nurnberg G, Renne U, Bunger L (2002) Intrinsic properties of muscle satellite cells are changed in response to long-term selection of mice for different growth traits. Cell Tissue Res 310:339–348CrossRefGoogle Scholar
  40. 40.
    Langhammer M, Renne U, Zeissler A, Nürnberg G, Bielohuby M, Grass H, Barthuber C, Schmitz K, Baur C, Ritz-Timme S, Boege F, Sawitzky M, Brenmoehl J, Metzger F, Bidlingmaier M, Reinsch N, Hoeflich A (2012) Severe reductions of life-span in giant mouse lines long-term selected for high growth. In: Proceedings of 55th symposium of the German endocrine society 7–10 March 2012, Mannheim, GermanyGoogle Scholar
  41. 41.
    Rehfeldt C, Bünger L (1990) Effects of long-term selection of laboratory mice on parameters of muscle growth and muscle structure. Arch Tierz-Arch Anim Breed 33:507–516Google Scholar
  42. 42.
    Renne U, Langhammer M (1999) Selection response after long-term selection for high and low running activity in mice with special consideration of a selection limit. In: Proceedings of 50th annnual meeting EAAP, Zürich, Schweiz 12; 58Google Scholar
  43. 43.
    Vanselow J, Kucia M, Langhammer M, Koczan D, Rehfeldt C, Metges CC (2011) Hepatic expression of the GH/JAK/STAT/IGF pathway, acute-phase response signalling and complement system are affected in mouse offspring by prenatal and early postnatal exposure to maternal high-protein diet. Eur J Nutr 50:611–623CrossRefGoogle Scholar
  44. 44.
    Rehfeldt C, Te Pas MFW, Wimmers K, Brameld JM, Nissen PM, Berri C, Valente LMP, Power DM, Picard B, Stickland NC, Oksbjerg N (2011) Advances in research on the prenatal development of skeletal muscle in animals in relation to the quality of muscle-based food. I. Regulation of myogenesis and environmental impact. Animal 5:703–717CrossRefGoogle Scholar
  45. 45.
    Kuhla B, Kucia M, Görs S, Albrecht D, Langhammer M, Kuhla S, Metges CC (2010) Effect of a high-protein diet on food intake and liver metabolism during pregnancy, lactation and after weaning in mice. Proteomics 10:2573–2588CrossRefGoogle Scholar
  46. 46.
    Campbell WW, Crim MC, Young VR, Evans WJ (1994) Increased energy requirements and changes in body composition with resistance training in older adults. Am J Clin Nutr 60:167–175Google Scholar
  47. 47.
    Rehfeldt C, Fiedler I, Stickland NC (2004) Number and size of muscle fibres in relation to meat production. In: Te Pas MFW, Haagsman ME, Everts HP (eds) Muscle development of livestock animals: physiology, genetics, and meat quality. CAB Int, Wallingford, Oxon, pp 1–37CrossRefGoogle Scholar
  48. 48.
    Moss FP, Leblond CP (1971) Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec 170:421–435CrossRefGoogle Scholar
  49. 49.
    Schultz E (1974) A quantitative study of the satellite cell population in postnatal mouse lumbrical muscle. Anat Rec 180:589–595CrossRefGoogle Scholar
  50. 50.
    Miyazaki M, Esser KA (2009) Cellular mechanisms regulating protein synthesis and skeletal muscle hypertrophy in animals. J Appl Physiol 106:1367–1373CrossRefGoogle Scholar
  51. 51.
    Rehfeldt C, Fiedler I (1984) Postnatal development of muscle fibers in growing skeletal muscles of laboratory mice. Arch Exp Vet-med 38:178–192Google Scholar
  52. 52.
    Rayne J, Crawford GN (1975) Increase in fibre numbers of the rat pterygoid muscles during postnatal growth. J Anat 119:347–357Google Scholar
  53. 53.
    Summers PJ, Medrano JF (1997) Delayed myogenesis associated with muscle fiber hyperplasia in high-growth mice. Proc Soc Exp Biol Med 214:380–385Google Scholar
  54. 54.
    Glore SR, Layman DK (1983) Cellular development of skeletal muscle during early periods of nutritional restriction and subsequent rehabilitation. Ped Res 17:602–605CrossRefGoogle Scholar
  55. 55.
    Timson BF (1982) The effect of varying postnatal growth rate on skeletal muscle fiber number in the mouse. Growth 46:36–45Google Scholar
  56. 56.
    Rehfeldt C, Aner K, Bünger L (1991) Cellular response of skeletal muscle to nutritional restriction in laboratory mice. Arch Tierz-Arch Anim Breed 34:429–439Google Scholar
  57. 57.
    Bayol SA, Simbi BH, Stickland NC (2005) A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567:951–961CrossRefGoogle Scholar
  58. 58.
    Wittstock M, Rehfeldt C, Nürnberg G, Renne U, Bruck W, Mix E, Zettl UK (2003) Susceptibility to apoptosis in different murine muscle cell lines. J Muscle Res Cell Motil 24:521–526CrossRefGoogle Scholar
  59. 59.
    Hardie DG, Sakamoto K (2006) AMPK: a key sensor of fuel and energy status in skeletal muscle. Physiology (Bethesda) 21:48–60CrossRefGoogle Scholar
  60. 60.
    Jorgensen SB, Richter EA, Wojtaszewski JF (2006) Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 574:17–31CrossRefGoogle Scholar
  61. 61.
    Gondret F, Lebret B (2002) Feeding intensity and dietary protein level affect adipocyte cellularity and lipogenic capacity of muscle homogenates in growing pigs, without modification of the expression of sterol regulatory element binding protein. J Anim Sci 80:3184–3193Google Scholar
  62. 62.
    Jouaville LF, Fellmann N, Coudert J, Clottes E (2006) Skeletal muscle expression of LDH and monocarboxylate transporters in growing rats submitted to protein malnutrition. Eur J Nutr 45:355–362CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Charlotte Rehfeldt
    • 1
  • Martina Langhammer
    • 2
  • Marzena Kucia
    • 3
  • Gerd Nürnberg
    • 2
  • Cornelia C. Metges
    • 3
  1. 1.Research Unit Muscle Biology and GrowthLeibniz Institute for Farm Animal Biology (FBN)DummerstorfGermany
  2. 2.Research Unit Genetics and BiometryDummerstorfGermany
  3. 3.Research Unit Nutritional PhysiologyLeibniz Institute for Farm Animal Biology (FBN)DummerstorfGermany

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