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Cultured neonatal rat cardiomyocytes display differences in glucose uptake and sensitivity to dexamethasone related to maternal diet

Published online by Cambridge University Press:  21 April 2011

R. M. Austin  and
S. C. Langley-Evans
R. M. Austin
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, UK
S. C. Langley-Evans*
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, UK
*
*Address for correspondence: Prof S. C. Langley-Evans, School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, LE12 5RD, UK. (Email [email protected])
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Abstract

Feeding a low protein (LP) diet in rat pregnancy is associated with impaired cardiovascular health and function, possibly as a result of tissue remodelling. To assess whether cardiomyocytes retain differences induced by protein restriction, cells from neonatal rats exposed to control or LP diets in utero were cultured for a period of 10 days. At the end of this period, no differences in cell size, proliferation differentiation or metabolic function were noted. When treated with dexamethasone (0.1–10 μM) for 2 days, it was noted that insulin-stimulated glucose uptake was enhanced, but only in cells from LP rats. Increased glucocorticoid sensitivity of cardiomyocytes from LP rats could not be explained by differential expression of the glucocorticoid receptor or the glucose transporters, GLUT1 and GLUT4. The findings of the study suggest that sensitivity to endocrine signals may be permanently programmed by undernutrition through mechanisms that are preserved in vitro.

Keywords

cardiomyocytescell culturedexamethasoneprogramming
Type
Brief Report
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Issue 3 , June 2011 , pp. 190 - 194
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

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References

1. Langley-Evans, SC. Nutritional programming of disease: unravelling the mechanism. J Anat. 2009; 215, 36–51.CrossRefGoogle ScholarPubMed
2. Langley, SC, Jackson, AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond). 1994; 86, 217–222.CrossRefGoogle ScholarPubMed
3. Swali, A, McMullen, S, Langley-Evans, SC. Prenatal protein restriction leads to a disparity between aortic and peripheral blood pressure in Wistar male offspring. J Physiol. 2010; 588, 3809–3818.CrossRefGoogle ScholarPubMed
4. Yates, Z, Tarling, EJ, Langley-Evans, SC, Salter, AM. Maternal undernutrition programmes atherosclerosis in the ApoE*3-Leiden mouse. Br J Nutr. 2009; 101, 1185–1194.CrossRefGoogle ScholarPubMed
5. Torrens, C, Brawley, L, Anthony, FW, et al. Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension. 2006; 47, 982–987.CrossRefGoogle ScholarPubMed
6. Elmes, MJ, Gardner, DS, Langley-Evans, SC. Fetal exposure to a maternal low-protein diet is associated with altered left ventricular pressure response to ischaemia-reperfusion injury. Br J Nutr. 2007; 98, 93–100.CrossRefGoogle ScholarPubMed
7. Cheema, KK, Dent, MR, Saini, HK, Aroutiounova, N, Tappia, PS. Prenatal exposure to maternal undernutrition induces adult cardiac dysfunction. Br J Nutr. 2005; 93, 471–477.CrossRefGoogle ScholarPubMed
8. Corstius, HB, Zimanyi, MA, Maka, N, et al. Effect of intrauterine growth restriction on the number of cardiomyocytes in rat hearts. Pediatr Res. 2005; 57, 796–800.CrossRefGoogle ScholarPubMed
9. Slater-Jefferies, JL, Lillycrop, KA, Townsend, PA, et al. Feeding a protein-restricted diet during pregnancy induces altered epigenetic regulation of peroxisomal proliferator-activated receptor-α in the heart of the offspring. Journal of Developmental Origins of Health and Disease. 2011 (in press).CrossRefGoogle ScholarPubMed
10. Gluckman, PD, Hanson, MA, Buklijas, T, Low, FM, Beedle, AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol. 2009; 5, 401–408.CrossRefGoogle ScholarPubMed
11. Seckl, JR, Holmes, MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 2007; 3, 479–488.CrossRefGoogle ScholarPubMed
12. Bogdarina, I, Haase, A, Langley-Evans, S, Clark, AJ. Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS One. 2010; 5, e9237.CrossRefGoogle ScholarPubMed
13. McMullen, S, Gardner, DS, Langley-Evans, SC. Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br J Nutr. 2004; 91, 133–140.CrossRefGoogle ScholarPubMed
14. Baram, TZ, Schultz, L. Fetal and maternal levels of corticosterone after pharmacological adrenalectomy. Life Sci. 1990; 47, 485–489.CrossRefGoogle ScholarPubMed
15. Bradford, MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72, 248–254.CrossRefGoogle ScholarPubMed
16. Labarca, C, Paigen, K. A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980; 102, 344–352.CrossRefGoogle ScholarPubMed
17. Kozma, L, Baltensperger, K, Klarlund, J, et al. The ras signaling pathway mimics insulin action on glucose transporter translocation. Proc Natl Acad Sci U S A. 1993; 90, 4460–4464.CrossRefGoogle ScholarPubMed
18. Cornock, R, Langley-Evans, SC, Mobasheri, A, McMullen, S. The impact of maternal protein restriction during rat pregnancy upon renal expression of angiotensin receptors and vasopressin-related aquaporins. Reprod Biol Endocrinol. 2010; 8, 105–110.CrossRefGoogle ScholarPubMed
19. Yan, J, Young, ME, Cui, L, et al. Increased glucose uptake and oxidation in mouse hearts prevent high fatty acid oxidation but cause cardiac dysfunction in diet induced obesity. Circulation. 2009; 119, 2818–2828.CrossRefGoogle ScholarPubMed
20. Aroutiounova, N, Fandrich, R, Kardami, E, Tappia, PS. Prenatal exposure to maternal low protein diet suppresses replicative potential of myocardial cells. Nutr Metab Cardiovasc Dis. 2009; 19, 707–712.CrossRefGoogle ScholarPubMed
21. Porrello, ER, Meeker, WF, Thomas, WE, Widdop, E, Delbridge, LM. Glucocorticoids suppress growth in neonatal cardiomyocytes co-expressing angiotensin (2) and angiotensin (1) receptors. Neonatology. 2010; 97, 257–265.CrossRefGoogle Scholar
22. Lister, K, Autelitano, DJ, Jenkins, A, Hannan, RD, Sheppard, KE. Cross talk between corticosteroids and alpha adrenergic signalling augments cardiomyocyte hypertrophy: a role for SGK1. Cardiovasc Res. 2006; 70, 555–565.CrossRefGoogle ScholarPubMed
23. Studelska, DR, Campbell, C, Pang, S, Rodnick, KJ, James, DE. Developmental expression of insulin-regulatable glucose transporter GLUT-4. Am J Physiol. 1992; 263, E102–E106.Google ScholarPubMed
24. Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R368–R373.CrossRefGoogle ScholarPubMed
25. Ozanne, SE, Olsen, GS, Hansen, LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003; 177, 235–241.CrossRefGoogle ScholarPubMed