Effects of Maternal Diet and Exercise during Pregnancy on Glucose Metabolism in Skeletal Muscle and Fat of Weanling Rats
Open accessAbstract
Obesity during pregnancy contributes to the development of metabolic disorders in offspring. Maternal exercise may limit gestational weight gain and ameliorate these programming effects. We previously showed benefits of post-weaning voluntary exercise in offspring from obese dams. Here we examined whether voluntary exercise during pregnancy influences lipid and glucose homeostasis in muscle and fat in offspring of both lean and obese dams. Female Sprague-Dawley rats were fed chow (C) or high fat (F) diet for 6 weeks before mating. Half underwent voluntary exercise (CE/FE) with a running wheel introduced 10 days prior to mating and available until the dams delivered; others remained sedentary (CS/FS). Male and female pups were killed at postnatal day (PND)19 and retroperitoneal fat and gastrocnemius muscle were collected for gene expression. Lean and obese dams achieved similar modest levels of exercise. At PND1, both male and female pups from exercised lean dams were significantly lighter (CE versus CS), with no effect in those from obese dams. At PND19, maternal obesity significantly increased offspring body weight and adiposity, with no effect of maternal exercise. Exercise significantly reduced insulin concentrations in males (CE/FE versus CS/FS), with reduced glucose in male FE pups. In males, maternal obesity significantly decreased muscle myogenic differentiation 1 (MYOD1) and glucose transporter type 4 (GLUT4) mRNA expressions (FS vs CS); these were normalized by exercise. Maternal exercise upregulated adipose GLUT4, interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-α), and peroxisome proliferator activated receptor gamma coactivator 1 alpha (PGC1α) mRNA expression in offspring of dams consuming chow. Modest voluntary exercise during pregnancy was associated with lower birth weight in pups from lean dams. Maternal exercise appeared to decrease the metabolic risk induced by maternal obesity, improving insulin/glucose metabolism, with greater effects in male than female offspring.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Programmed changes in offspring adipose biology may be permanent, as an exercise intervention in mothers fed a high-fat diet did not prevent the increased adiposity or trigger beneficial changes in insulin signaling component expression in their fetuses.
“some research suggests that programmed changes in offspring adipose biology may be permanent, as an exercise intervention in mothers fed a high-fat diet did not prevent the increased adiposity or trigger beneficial changes in insulin signaling component expression in their fetuses [95].”
From Developmental programming of offspring adipose tissue biology and obesity risk (2021) · cites this paper as [95]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The anti-inflammatory effect of exercise
Petersen, A. M. W., & Pedersen, B. K. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00164.2004 · Cited by 3,100 · cited 1× · see citing works
“In addition, IL-6 has strong anti-inflammatory effects and may inhibit TNF-α induced insulin resistance [60].”
BackgroundPeroxisome proliferator–activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis
Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., & Kelly, D. P. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10268 · Cited by 1,285 · see citing works
Reynolds, R. M., Allan, K. M., Raja, E. A., Bhattacharya, S., McNeill, G., Hannaford, P. C., Sarwar, N., Lee, A. J., Bhattacharya, S., & Norman, J. E. (2013) · BMJ · doi:10.1136/bmj.f4539 · Cited by 571 · see citing works
Kennedy, J. W., Hirshman, M. F., Gervino, E. V., Ocel, J. V., Forse, R. A., Hoenig, S. J., Aronson, D., Goodyear, L. J., & Horton, E. S. (1999) · Diabetes · doi:10.2337/diabetes.48.5.1192 · Cited by 415 · see citing works
Obesity, pregnancy, inflammation, and vascular function
Denison, F. C., Roberts, K. A., Barr, S. M., & Norman, J. E. (2010) · Reproduction · doi:10.1530/rep-10-0074 · Cited by 221 · see citing works
Nutrition and Exercise Prevent Excess Weight Gain in Overweight Pregnant Women
MOTTOLA, M. F., GIROUX, I., GRATTON, R., HAMMOND, J.-A., HANLEY, A., HARRIS, S., MCMANUS, R., DAVENPORT, M. H., & SOPPER, M. M. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181b5419a · Cited by 171 · see citing works
Alfaradhi, M. Z., Fernandez-Twinn, D. S., Martin-Gronert, M. S., Musial, B., Fowden, A., & Ozanne, S. E. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00049.2014 · Cited by 136 · see citing works
Maternal exercise improves insulin sensitivity in mature rat offspring
CARTER, L. G., QI, N. R., CABO, R. D., & PEARSON, K. J. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31827de953 · Cited by 121 · see citing works
Flagged first, then by citations
Research works printed but not linked: 52
- [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. 10.1001/jama.2012.39 22253363 · DOI
- [2]Begum KS, Sachchithanantham K, De Somsubhra S (2011) Maternal obesity and pregnancy outcome. Clin Exp Obstet Gynecol 38: 14– 20. 21485717
- [3]Cedergren MI (2004) Maternal morbid obesity and the risk of adverse pregnancy outcome. Obstet Gynecol 103: 219– 224. 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. 11236410 PMC1446581
- [5]Oken E, Taveras EM, Kleinman KP, Rich-Edwards JW, Gillman MW (2007) Gestational weight gain and child adiposity at age 3 years. Am J Obstet Gynecol 196: 322.e321– 328. 17403405 PMC1899090
- [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. 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 10.1371/journal.pone.0077809 24204979 PMC3817352 · DOI
- [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. 10.2337/dc08-0432 18535193 PMC2518362 · DOI
- [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. 10.1038/ijo.2008.213 18982008 · DOI
- [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. 16020464 PMC1474235
- [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. 10.1111/j.1365-2826.2010.02005.x 20403085 · DOI
- [14]Taylor PD, Poston L (2007) Developmental programming of obesity in mammals. Exp Physiol 92: 287– 298. 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. 10.1007/s00394-008-0760-5 19099241 · DOI
- [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. 10.1016/j.numecd.2010.11.007 21208789 · DOI
- [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. 10.1210/en.2012-2255 23959936 PMC3800750 · DOI · Paper page
- [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. 10.1042/CS20100534 21288203 · DOI
- [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. 10.1016/j.numecd.2011.12.009 22305126 · DOI
- [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. 10.1210/en.2013-1059 23928377 · DOI
- [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. 10.1111/jne.12053 23701669 · DOI
- [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. 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. 10.1111/j.1463-1326.2011.01426.x 21615668 · DOI
- [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. PMC3925765 23949616
- [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. 20413424
- [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. 20157566 PMC2815736
- [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. 10.1210/jc.2013-1943 23956348 PMC3790616 · DOI
- [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 10.1371/journal.pone.0024068 21901160 PMC3162035 · DOI
- [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 12184808 PMC126239
- [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. 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 10.1371/journal.pone.0006259 19606226 PMC2707610 · DOI
- [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. 12213876
- [34]Tremblay A, Simoneau J-A, Bouchard C (1994) Impact of exercise intensity on body fatness and skeletal muscle metabolism. Metabolism 43: 814– 818. 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. 23224031
- [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. 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. 19657097
- [38]Cunningham SA, Kramer MR, Narayan KMV (2014) Incidence of Childhood Obesity in the United States. New England Journal of Medicine 370: 403– 411. 10.1056/NEJMoa1309753 24476431 PMC4017620 · DOI
- [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. 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. 10753147 PMC27335
- [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. 10.1210/en.2008-0582 18635655 · DOI
- [42]Zambrano E, Nathanielsz PW (2013) Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutrition Reviews 71: S42– S54. 10.1111/nure.12068 24147924 · DOI
- [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. 20335449
- [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. 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. 11120515
- [47]Wells JC, Siervo M (2011) Obesity and energy balance: is the tail wagging the dog? Eur J Clin Nutr 65: 1173– 1189. 10.1038/ejcn.2011.132 21772313 · DOI
- [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. 7814644 PMC295454
- [51]Handschin C (2009) The biology of PGC-1alpha and its therapeutic potential. Trends Pharmacol Sci 30: 322– 329. 10.1016/j.tips.2009.03.006 19446346 · DOI · Paper page
- [52]Eisele PS, Handschin C (2014) Functional crosstalk of PGC-1 coactivators and inflammation in skeletal muscle pathophysiology. Semin Immunopathol 36: 27– 53. 10.1007/s00281-013-0406-4 24258516 · DOI
- [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. 10.1113/jphysiol.2008.165464 19221126 PMC2678229 · DOI
- [55]Liang H, Ward WF (2006) PGC-1α: a key regulator of energy metabolism. Advances in Physiology Education 30: 145– 151. 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. 10.1152/ajpendo.90924.2008 19176350 PMC2670630 · DOI
- [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. 10.1095/biolreprod.109.077099 19516021 PMC2802110 · DOI
- [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. 10.1016/j.earlhumdev.2013.09.014 24090868 · DOI
- [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. 10.1007/s12519-011-0292-6 21874618 · DOI
Cited by
Sorted by citations
Developmental programming of offspring adipose tissue biology and obesity risk
Rodgers, A., & Sferruzzi-Perri, A. N. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00790-w · Cited by 57 · see citing works
Uddin, G. M., Youngson, N. A., Chowdhury, S. S., Hagan, C., Sinclair, D. A., & Morris, M. J. (2020) · Cells · doi:10.3390/cells9040791 · Cited by 32 · see citing works
Self-citationQuiclet, C., Dubouchaud, H., Berthon, P., Sanchez, H., Vial, G., Siti, F., Fontaine, E., Batandier, C., & Couturier, K. (2017) · The Journal of Physiology · doi:10.1113/jp274739 · Cited by 31 · see citing works
- Authors
- Raipuria, M., Bahari, H., & Morris, M. J.
- Affiliations
- UNSW Sydney (AU)
- Universiti Putra Malaysia (MY)
- Corresponding author
- Morris, Margaret J.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-04-08
- Volume
- 10
- Issue
- 4
- Pages
- e0120980
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4390148
- OpenAlex
- W2019155361
- Cited by
- 90
- References
- 8
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 14 · 2021: 13 · 2020: 13 · 2019: 6 · 2018: 8 · 2017: 11 · 2016: 7 · 2015: 4
- FWCI
- 9.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- UNSWorks (University of New South Wales, Sydney, Australia) (submittedVersion, cc-by)
- Greater South Information System
- Funders
- University of New South Wales
- Universiti Putra Malaysia
- Medical Research Council
- National Health and Medical Research Council (568728)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
- Keywords
- maternal obesity, exercise during pregnancy, maternal diet, high-fat diet, gestational weight gain, insulin resistance, GLUT4, MyoD, skeletal muscle, adipose tissue, PGC-1α, interleukin-6, TNF-α, birth weight, sex differences, developmental programming, weanling rats
- MeSH terms
- Adipose Tissue, Animals, Diet, Female, Gene Expression Regulation, Glucose, Hormones, Insulin, Male, Mothers, Obesity, Organ Size, Phenotype, Physical Conditioning, Animal, Pregnancy, Triglycerides, Weaning, Biomarkers, Rats, Sprague-Dawley, Muscle, Skeletal, Rats, Adipose Tissue, White
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review