Effects of maternal diet and exercise during pregnancy on glucose metabolism in skeletal muscle and fat of weanling rats

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Raipuria, Mukesh ^a   Bahari, Hasnah ^a,b   Morris, Margaret J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY PUTRA MALAYSIA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER; HORMONE;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALORIC INTAKE; EXERCISE; FEMALE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; INSULIN BLOOD LEVEL; LIPID HOMEOSTASIS; MALE; MATERNAL NUTRITION; MATERNAL OBESITY; MOUSE; MUSCLE MASS; NONHUMAN; PHENOTYPE; PROGENY; RETROPERITONEAL FAT; SEDENTARY LIFESTYLE; SKELETAL MUSCLE; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BLOOD; DIET; GENE EXPRESSION REGULATION; METABOLISM; MOTHER; OBESITY; ORGAN SIZE; PATHOPHYSIOLOGY; PREGNANCY; RAT; SPRAGUE DAWLEY RAT; WEANING; WHITE ADIPOSE TISSUE;

RATTUS;

ADIPOSE TISSUE; ADIPOSE TISSUE, WHITE; ANIMALS; BIOMARKERS; DIET; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; HORMONES; INSULIN; MALE; MOTHERS; MUSCLE, SKELETAL; OBESITY; ORGAN SIZE; PHENOTYPE; PHYSICAL CONDITIONING, ANIMAL; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; TRIGLYCERIDES; WEANING;

EID: 84928910722     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120980     Document Type: Article

References (60)

1. Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) PRevalence of obesity and trends in the distribution of body mass index among us adults, 1999-2010. JAMA 307: 491-497. doi: 10.1001/jama.2012.39 PMID: 22253363
2. Begum KS, Sachchithanantham K, De Somsubhra S (2011) Maternal obesity and pregnancy outcome. Clin Exp Obstet Gynecol 38: 14-20. PMID: 21485717
3. Cedergren MI (2004) Maternal morbid obesity and the risk of adverse pregnancy outcome. Obstet Gynecol 103: 219-224. PMID: 14754687
4. Baeten JM, Bukusi EA, Lambe M (2001) Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 91: 436-440. PMID: 11236410
5. Oken E, Taveras EM, Kleinman KP, Rich-Edwards JW, GillmanMW(2007) Gestational weight gain and child adiposity at age 3 years. Am J Obstet Gynecol 196: 322.e321-328. PMID: 17403405
6. Denison FC, Roberts KA, Barr SM, Norman JE (2010) Obesity, pregnancy, inflammation, and vascular function. Reproduction 140: 373-385. doi: 10.1530/REP-10-0074 PMID: 20215337
7. Parsons TJ, Power C, Logan S, Summerbell CD (1999) Childhood predictors of adult obesity: a systematic review. Int J Obes Relat Metab Disord 23 Suppl 8: S1-107. PMID: 10641588
8. Li N, Liu E, Guo J, Pan L, Li B, Wang P, et al. (2013) Maternal Prepregnancy Body Mass Index and Gestational Weight Gain on Offspring Overweight in Early Infancy. PLoS ONE 8: e77809. doi: 10. 1371/journal.pone.0077809 PMID: 24204979
9. Mingrone G, Manco M, Valera Mora ME, Guidone C, Iaconelli A, Gniuli D, et al. (2008) Influence of Maternal Obesity on Insulin Sensitivity and Secretion in Offspring. Diabetes Care 31: 1872-1876. doi: 10. 2337/dc08-0432 PMID: 18535193
10. Alfaradhi MZ, Fernandez-Twinn DS, Martin-Gronert MS, Musial B, Fowden AL, Ozanne SE (2014) Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity: Am J Physiol Reg Integr Comp Physiol. doi: 10.1152/ajpregu.00049.02014 p. PMID: 24789994
11. Morris MJ, Chen H (2009) Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int J Obes (Lond) 33: 115-122. doi: 10.1038/ijo.2008.213 PMID: 18982008
12. 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. The Journal of Physiology 567: 951-961. PMID: 16020464
13. Rajia S, Chen H, Morris MJ (2010) Maternal Overnutrition Impacts Offspring Adiposity and Brain Appetite Markers-Modulation by Postweaning Diet. Journal of neuroendocrinology 22: 905-914. doi: 10. 1111/j.1365-2826.2010.02005.x PMID: 20403085
14. Taylor PD, Poston L (2007) Developmental programming of obesity in mammals. Exp Physiol 92: 287-298. PMID: 17170060
15. Bayol S, Macharia R, Farrington S, Simbi B, Stickland N (2009) Evidence that a maternal "junk food" diet during pregnancy and lactation can reduce muscle force in offspring. European Journal of Nutrition 48: 62-65. doi: 10.1007/s00394-008-0760-5 PMID: 19099241
16. Simar D, Chen H, Lambert K, Mercier J, Morris MJ (2012) Interaction between maternal obesity and post-natal over-nutrition on skeletal muscle metabolism. Nutr Metab Cardiovasc Dis 22: 269-276. doi: 10.1016/j.numecd.2010.11.007 PMID: 21208789
17. Borengasser SJ, Zhong Y, Kang P, Lindsey F, Ronis MJJ, Badger TM, et al. (2013) Maternal Obesity Enhances White Adipose Tissue Differentiation and Alters Genome-Scale DNA Methylation in Male Rat Offspring. Endocrinology 154: 4113-4125. doi: 10.1210/en.2012-2255 PMID: 23959936
18. Benkalfat NB, Merzouk H, Bouanane S, Merzouk SA, Bellenger J, Gresti J, et al. (2011) Altered adipose tissue metabolism in offspring of dietary obese rat dams. Clinical Science 121: 19-28. doi: 10. 1042/CS20100534 PMID: 21288203
19. Rajia S, Chen H, Morris MJ (2013) Voluntary post weaning exercise restores metabolic homeostasis in offspring of obese rats. Nutrition, Metabolism and Cardiovascular Diseases 23: 574-581. doi: 10.1016/ j.numecd.2011.12.009 PMID: 22305126
20. Bahari H, Caruso V, Morris MJ (2013) Late-onset exercise in female rat offspring ameliorates the detrimental metabolic impact of maternal obesity. Endocrinology 154: 3610-3621. doi: 10.1210/en.2013-1059 PMID: 23928377
21. Caruso V, Bahari H, Morris MJ (2013) The Beneficial Effects of Early Short-Term Exercise in the Offspring of Obese Mothers are Accompanied by Alterations in the Hypothalamic Gene Expression of Appetite Regulators and FTO (Fat Mass and Obesity Associated) Gene. Journal of neuroendocrinology 25: 742-752. doi: 10.1111/jne.12053 PMID: 23701669
22. Ren JM, Semenkovich CF, Gulve EA, Gao J, Holloszy JO (1994) Exercise induces rapid increases in GLUT4 expression, glucose transport capacity, and insulin-stimulated glycogen storage in muscle. Journal of Biological Chemistry 269: 14396-14401. PMID: 8182045
23. Hussey SE, McGee SL, Garnham A, Wentworth JM, Jeukendrup AE, Hargreaves M (2011) Exercise training increases adipose tissue GLUT4 expression in patients with type 2 diabetes. Diabetes, Obesity and Metabolism 13: 959-962. doi: 10.1111/j.1463-1326.2011.01426.x PMID: 21615668
24. Carter LG, Qi NR, De Cabo R, Pearson KJ (2013) Maternal exercise improves insulin sensitivity in mature rat offspring. Med Sci Sports Exerc 45: 832-840. doi: 10.1249/MSS.0b013e31827de953 PMID: 23247711
25. Vega CC, Reyes-Castro LA, Bautista CJ, Larrea F, Nathanielsz PW, Zambrano E (2013) Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes.
26. Hokari F, Kawasaki E, Sakai A, Koshinaka K, Sakuma K, Kawanaka K (2010) Muscle contractile activity regulates Sirt3 protein expression in rat skeletal muscles. J Appl Physiol (1985) 109: 332-340.
27. Palacios OM, Carmona JJ, Michan S, Chen KY, Manabe Y, Ward JL 3rd, et al. (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1alpha in skeletal muscle. Aging (Albany NY) 1: 771-783. PMID: 20157566
28. Boyle KE, Newsom SA, Janssen RC, Lappas M, Friedman JE (2013) Skeletal muscle MnSOD, mitochondrial complex II, and SIRT3 enzyme activities are decreased in maternal obesity during human pregnancy and gestational diabetes mellitus. J Clin Endocrinol Metab 98: E1601-1609. doi: 10.1210/ jc.2013-1943 PMID: 23956348
29. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJ, Badger TM, et al. (2011) Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 6: e24068. doi: 10.1371/journal.pone.0024068 PMID: 21901160
30. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: Research0034. PMID: 12184808
31. 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. PMID: 11846609
32. Chen H, Simar D, Morris MJ (2009) Hypothalamic Neuroendocrine Circuitry is Programmed by Maternal Obesity: Interaction with Postnatal Nutritional Environment. PLoS ONE 4: e6259. doi: 10.1371/ journal.pone.0006259 PMID: 19606226
33. Ramsay JE, Ferrell WR, Crawford L, Wallace AM, Greer IA, Sattar N (2002) Maternal Obesity Is Associated with Dysregulation of Metabolic, Vascular, and Inflammatory Pathways. The Journal of Clinical Endocrinology & Metabolism 87: 4231-4237.
34. Tremblay A, Simoneau J-A, Bouchard C (1994) Impact of exercise intensity on body fatness and skeletal muscle metabolism. Metabolism 43: 814-818. PMID: 8028502
35. Chan C-Y, Kendig M, Boakes R, Rooney K (2013) Low-volume exercise can prevent sucrose-induced weight gain but has limited impact on metabolic measures in rats. Eur J Clin Nutr 52: 1721-1732.
36. Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, Badger TM (2008) Maternal obesity at conception programs obesity in the offspring. American journal of physiology Regulatory, integrative and comparative physiology 294: R528-538. PMID: 18032473
37. Page KC, Malik RE, Ripple JA, Anday EK (2009) Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 297: R1049-R1057.
38. Cunningham SA, Kramer MR, Narayan KMV (2014) Incidence of Childhood Obesity in the United States. New England Journal of Medicine 370: 403-411. doi: 10.1056/NEJMoa1309753 PMID: 24476431
39. Stettler N, Kumanyika SK, Katz SH, Zemel BS, Stallings VA (2003) Rapid weight gain during infancy and obesity in young adulthood in a cohort of African Americans. Am J Clin Nutr 77: 1374-1378. PMID: 12791612
40. Ong KKL, Ahmed ML, Emmett PM, Preece MA, Dunger DB (2000) Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 320: 967-971. PMID: 10753147
41. Chen H, Simar D, Lambert K, Mercier J, Morris MJ (2008) Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology 149: 5348-5356. doi: 10.1210/en. 2008-0582 PMID: 18635655
42. Zambrano E, Nathanielsz PW (2013) Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutrition Reviews 71: S42-S54. doi: 10.1111/nure.12068 PMID: 24147924
43. Hopkins SA, Baldi JC, Cutfield WS, McCowan L, Hofman PL (2010) Exercise Training in Pregnancy Reduces Offspring Size without Changes in Maternal Insulin Sensitivity. The Journal of Clinical Endocrinology & Metabolism 95: 2080-2088.
44. Bell RJ, Palma SM, Lumley JM (1995) The Effect of Vigorous Exercise During Pregnancy on Birth-Weight. Australian and New Zealand Journal of Obstetrics and Gynaecology 35: 46-51. PMID: 7771999
45. Clapp Iii JF, Kim H, Burciu B, Lopez B (2000) Beginning regular exercise in early pregnancy: Effect on fetoplacental growth. Am J Obstet Gynecol 183: 1484-1488. PMID: 11120515
46. Mottola MF, Giroux I, Gratton R, Hammond J-A, Hanley A, Harris S, et al. (2010) Nutrition and exercise prevent excess weight gain in overweight pregnant women. Med Sci Sports Exerc 42: 265. doi: 10. 1249/MSS.0b013e3181b5419a PMID: 20083959
47. Wells JC, Siervo M (2011) Obesity and energy balance: is the tail wagging the dog? Eur J Clin Nutr 65: 1173-1189. doi: 10.1038/ejcn.2011.132 PMID: 21772313
48. Reynolds RM, Allan KM, Raja EA, Bhattacharya S, McNeill G, Hannaford PC, et al. (2013) Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: followup of 1 323 275 person years. BMJ 347.
49. Kennedy JW, Hirshman MF, Gervino EV, Ocel JV, Forse RA, Hoenig SJ, et al. (1999) Acute exercise induces GLUT4 translocation in skeletal muscle of normal human subjects and subjects with type 2 diabetes. Diabetes 48: 1192-1197. PMID: 10331428
50. Ren JM, Marshall BA, Mueckler MM, McCaleb M, Amatruda JM, Shulman GI (1995) Overexpression of Glut4 protein in muscle increases basal and insulin-stimulated whole body glucose disposal in conscious mice. J Clin Invest 95: 429-432. PMID: 7814644
51. Handschin C (2009) The biology of PGC-1alpha and its therapeutic potential. Trends Pharmacol Sci 30: 322-329. doi: 10.1016/j.tips.2009.03.006 PMID: 19446346
52. Eisele PS, Handschin C (2014) Functional crosstalk of PGC-1 coactivators and inflammation in skeletal muscle pathophysiology. Semin Immunopathol 36: 27-53. doi: 10.1007/s00281-013-0406-4 PMID: 24258516
53. Sutherland LN, Bomhof MR, Capozzi LC, Basaraba SAU, Wright DC (2009) Exercise and adrenaline increase PGC-1α mRNA expression in rat adipose tissue. The Journal of Physiology 587: 1607-1617. doi: 10.1113/jphysiol.2008.165464 PMID: 19221126
54. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP (2000) Peroxisome proliferator-activated receptor ã coactivator-1 promotes cardiac mitochondrial biogenesis. The Journal of Clinical Investigation 106: 847-856. PMID: 11018072
55. Liang H, Ward WF (2006) PGC-1α: a key regulator of energy metabolism. Advances in Physiology Education 30: 145-151. PMID: 17108241
56. Tong JF, Yan X, Zhu MJ, Ford SP, Nathanielsz PW, Du M (2009) Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle. Am J Physiol Endocrinol Metab 296: E917-924. doi: 10.1152/ajpendo.90924.2008 PMID: 19176350
57. Du M, Yan X, Tong JF, Zhao J, Zhu MJ (2010) Maternal Obesity, Inflammation, and Fetal Skeletal Muscle Development. Biology of Reproduction 82: 4-12. doi: 10.1095/biolreprod.109.077099 PMID: 19516021
58. van der Burg JW, Allred EN, McElrath TF, Fichorova RN, Kuban K, O'Shea TM, et al. (2013) Is maternal obesity associated with sustained inflammation in extremely low gestational age newborns? Early Human Development 89: 949-955. doi: 10.1016/j.earlhumdev.2013.09.014 PMID: 24090868
59. Leibowitz K, Moore R, Ahima R, Stunkard A, Stallings V, Berkowitz R, et al. (2012) Maternal obesity associated with inflammation in their children. World Journal of Pediatrics 8: 76-79. doi: 10.1007/s12519-011-0292-6 PMID: 21874618
60. Petersen AMW, Pedersen BK (2005) The anti-inflammatory effect of exercise. Journal of Applied Physiology 98: 1154-1162. PMID: 15772055