Gestational exercise protects adult male offspring from high-fat diet-induced hepatic steatosis

Journal of Hepatology

Volumn 64, Issue 1, 2016, Pages 171-178

  Sheldon, Ryan D ^a,b   Nicole Blaize, A ^c   Fletcher, Justin A ^a,b   Pearson, Kevin J ^e   Donkin, Shawn S ^d   Newcomer, Sean C ^f   Rector, R Scott ^a,b  

^a University of Missouri   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c PURDUE UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

^e UNIVERSITY OF KENTUCKY   (United States)

^f NONE   (United States)

Author keywords

Fetal origins; NAFLD; Rat

Indexed keywords

AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 5; BIOLOGICAL MARKER; CARBOHYDRATE; FAT; MEMBRANE PROTEIN; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CARRIER PROTEIN; PPARGC1A PROTEIN, RAT; TRANSCRIPTION FACTOR;

ADULT; ANIMAL EXPERIMENT; AREA UNDER THE CURVE; ARTICLE; AUTOPHAGY; BIRTH WEIGHT; BODY FAT; CHOW DIET; CONCEPTION; CONTROLLED STUDY; DIET; EXERCISE; FATTY LIVER; FEMALE; GESTATIONAL AGE; GLUCOSE TOLERANCE TEST; LIPID DIET; LITTER SIZE; MALE; MARE; MATERNAL EXERCISE; MITOCHONDRIAL BIOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROGENY; RAT; RUNNING; WEANING; WEIGHT GAIN; ANIMAL; NON-ALCOHOLIC FATTY LIVER DISEASE; PREGNANCY; SPRAGUE DAWLEY RAT;

ANIMALS; CARRIER PROTEINS; DIET, HIGH-FAT; FEMALE; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PHYSICAL CONDITIONING, ANIMAL; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTORS;

EID: 84953302262     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.08.022     Document Type: Article

References (47)

1. L.M. Mudd, K.M. Owe, M.F. Mottola, and J.M. Pivarnik Health benefits of physical activity during pregnancy: an international perspective Med Sci Sports Exerc 45 2013 268 277
2. K.M. Borodulin, K.R. Evenson, F. Wen, A.H. Herring, and A.M. Benson Physical activity patterns during pregnancy Med Sci Sports Exerc 40 2008 1901 1908
3. P.L. Entin, and K.M. Munhall Recommendations regarding exercise during pregnancy made by private/small group practice obstetricians in the USA J Sport Sci Med 5 2006 449 458
4. P.D. Gluckman, M.A. Hanson, C. Cooper, and K.L. Thornburg Effect of in utero and early-life conditions on adult health and disease N Engl J Med 359 2008 61 73
5. P.D. Gluckman, and M.A. Hanson Developmental origins of disease paradigm: a mechanistic and evolutionary perspective Pediatr Res 56 2004 311 317
6. L.G. Carter, N.R. Qi, R. De Cabo, and K.J. Pearson Maternal exercise improves insulin sensitivity in mature rat offspring Med Sci Sports Exerc 45 2013 832 840
7. R.C. Laker, T.S. Lillard, M. Okutsu, M. Zhang, K.L. Hoehn, J.J. Connelly, and et al. Exercise prevents maternal high-fat diet-induced hypermethylation of the pgc-1alpha gene and age-dependent metabolic dysfunction in the offspring Diabetes 63 2014 1605 1611
8. K.I. Stanford, M.Y. Lee, K.M. Getchell, K. So, M.F. Hirshman, and L.J. Goodyear Exercise before and during pregnancy prevents the deleterious effects of maternal high-fat feeding on metabolic health of male offspring Diabetes 64 2015 427 433
9. L.G. Carter, K.N. Lewis, D.C. Wilkerson, C.M. Tobia, S.Y. Ngo Tenlep, P. Shridas, and et al. Perinatal exercise improves glucose homeostasis in adult offspring Am J Physiol Endocrinol Metab 303 2012 E1061 E1068
10. R.S. Rector, and J.P. Thyfault Does physical inactivity cause nonalcoholic fatty liver disease? J Appl Physiol 111 2011 1828 1835
11. J.D. Browning, L.S. Szczepaniak, R. Dobbins, P. Nuremberg, J.D. Horton, J.C. Cohen, and et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity Hepatology 40 2004 1387 1395
12. Z.M. Younossi, M. Stepanova, M. Afendy, Y. Fang, Y. Younossi, H. Mir, and et al. Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008 Clin Gastroenterol Hepatol 9 2011 524 530 e521; quiz e560
13. J.P. Ong, A. Pitts, and Z.M. Younossi Increased overall mortality and liver-related mortality in non-alcoholic fatty liver disease J Hepatol 49 2008 608 612
14. C.D. Byrne, and G. Targher Ectopic fat, insulin resistance, and nonalcoholic fatty liver disease: implications for cardiovascular disease Arterioscler Thromb Vasc Biol 34 2014 1155 1161
15. M.Z. Alfaradhi, D.S. Fernandez-Twinn, M.S. Martin-Gronert, B. Musial, A. Fowden, and S.E. Ozanne Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity Am J Physiol Regul Integr Comp Physiol 307 2014 R26 R34
16. E.M. Spangenberg, H. Augustsson, K. Dahlborn, B. Essen-Gustavsson, and K. Cvek Housing-related activity in rats: effects on body weight, urinary corticosterone levels, muscle properties and performance Lab Anim 39 2005 45 57
17. M.M. Tai A mathematical model for the determination of total area under glucose tolerance and other metabolic curves Diabetes Care 17 1994 152 154
18. R.S. Rector, J.P. Thyfault, R.T. Morris, M.J. Laye, S.J. Borengasser, F.W. Booth, and et al. Daily exercise increases hepatic fatty acid oxidation and prevents steatosis in Otsuka Long-Evans Tokushima Fatty rats Am J Physiol Gastrointest Liver Physiol 294 2008 G619 G626
19. S.S. Donkin, and L.E. Armentano Regulation of gluconeogenesis by insulin and glucagon in the neonatal bovine Am J Physiol 266 1994 R1229 R1237
20. I.G. Camarillo, L. Clah, W. Zheng, X. Zhou, B. Larrick, N. Blaize, and et al. Maternal exercise during pregnancy reduces risk of mammary tumorigenesis in rat offspring Eur J Cancer Prev 23 2014 502 505
21. A. Nicole Blaize, E. Breslin, S.S. Donkin, R. Cabot, K.J. Pearson, and S.C. Newcomer Maternal exercise does not significantly alter adult rat offspring vascular function Med Sci Sports Exerc 47 2015 2340 2346
22. M. Aharoni-Simon, M. Hann-Obercyger, S. Pen, Z. Madar, and O. Tirosh Fatty liver is associated with impaired activity of PPARgamma-coactivator 1alpha (pgc1alpha) and mitochondrial biogenesis in mice Lab Invest 91 2011 1018 1028
23. E.M. Morris, G.M. Meers, F.W. Booth, K.L. Fritsche, C.D. Hardin, J.P. Thyfault, and et al. Pgc-1α overexpression results in increased hepatic fatty acid oxidation with reduced triacylglycerol accumulation and secretion Am J Physiol Gastrointest Liver Physiol 303 2012 G979 G992
24. E.M. Morris, M.R. Jackman, G.M. Meers, G.C. Johnson, J.L. Lopez, P.S. MacLean, and et al. Reduced hepatic mitochondrial respiration following acute high-fat diet is prevented by pgc-1α overexpression Am J Physiol Gastrointest Liver Physiol 305 2013 G868 G880
25. R.S. Rector, J.P. Thyfault, G.M. Uptergrove, E.M. Morris, S.P. Naples, S.J. Borengasser, and et al. Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model J Hepatol 52 2010 727 736
26. E.M. Morris, M.R. Jackman, G.M. Meers, G.C. Johnson, J.L. Lopez, P.S. MacLean, and et al. Reduced hepatic mitochondrial respiration following acute high-fat diet is prevented by pgc-1alpha overexpression Am J Physiol Gastrointest Liver Physiol 305 2013 G868 G880
27. E.M. Morris, G.M. Meers, F.W. Booth, K.L. Fritsche, C.D. Hardin, J.P. Thyfault, and et al. Pgc-1alpha overexpression results in increased hepatic fatty acid oxidation with reduced triacylglycerol accumulation and secretion Am J Physiol Gastrointest Liver Physiol 303 2012 G979 G992
28. D. Glick, W. Zhang, M. Beaton, G. Marsboom, M. Gruber, M.C. Simon, and et al. Bnip3 regulates mitochondrial function and lipid metabolism in the liver Mol Cell Biol 32 2012 2570 2584
29. N. Mizushima, A. Yamamoto, M. Hatano, Y. Kobayashi, Y. Kabeya, K. Suzuki, and et al. Dissection of autophagosome formation using apg5-deficient mouse embryonic stem cells J Cell Biol 152 2001 657 667
30. T. Hanada, N.N. Noda, Y. Satomi, Y. Ichimura, Y. Fujioka, T. Takao, and et al. The atg12-atg5 conjugate has a novel e3-like activity for protein lipidation in autophagy J Biol Chem 282 2007 37298 37302
31. Y. Kabeya, N. Mizushima, T. Uero, A. Yamamoto, T. Kirisako, T. Noda, and et al. Lc3, a mammalian homologue of yeast apg8p, is localized in autophagosome membranes after processing EMBO J 19 2000 5720 5728
32. H.I. Mack, B. Zheng, J.M. Asara, and S.M. Thomas AMPK-dependent phosphorylation of ulk1 regulates atg9 localization Autophagy 8 2012 1197 1214
33. E. Morán-Salvador, M. López-Parra, V. García-Alonso, E. Titos, M. Martínez-Clemente, A. González-Périz, and et al. Role for PPARγ in obesity-induced hepatic steatosis as determined by hepatocyte-and macrophage-specific conditional knockouts FASEB J 25 2011 2538 2550
34. T. Shin, S. Kuboki, N. Huber, T. Eismann, E. Galloway, R. Schuster, and et al. Activation of peroxisome proliferator-activated receptor-gamma during hepatic ischemia is age-dependent J Surg Res 147 2008 200 205
35. F. Xu, J. Li, W. Ni, Y.W. Shen, and X.P. Zhang Peroxisome proliferator-activated receptor-gamma agonist 15d-prostaglandin j2 mediates neuronal autophagy after cerebral ischemia-reperfusion injury PLoS One 8 2013 e55080
36. D. Rovito, C. Giordano, D. Vizza, P. Plastina, I. Barone, I. Casaburi, and et al. Omega-3 PUFA ethanolamides DHEA and EPEA induce autophagy through PPARgamma activation in mcf-7 breast cancer cells J Cell Physiol 228 2013 1314 1322
37. A. Gonzalez-Rodriguez, R. Mayoral, N. Agra, M.P. Valdecantos, V. Pardo, M.E. Miquilena-Colina, and et al. Impaired autophagic flux is associated with increased endoplasmic reticulum stress during the development of NAFLD Cell Death Dis 5 2014 e1179
38. C.W. Lin, H. Zhang, M. Li, X. Xiong, X. Chen, X. Chen, and et al. Pharmacological promotion of autophagy alleviates steatosis and injury in alcoholic and non-alcoholic fatty liver conditions in mice J Hepatol 58 2013 993 999
39. M.M. Hussain, and A. Bakillah New approaches to target microsomal triglyceride transfer protein Curr Opin Lipidol 19 2008 572 578
40. D.W. Jun, J.H. Han, E.C. Jang, S.H. Kim, S.H. Kim, Y.J. Jo, and et al. Polymorphisms of microsomal triglyceride transfer protein gene and phosphatidylethanolamine n-methyltransferase gene in alcoholic and nonalcoholic fatty liver disease in Koreans Eur J Gastroenterol Hepatol 21 2009 667 672
41. M. Hashemi, H. Hoseini, P. Yaghmaei, A. Moazeni-Roodi, A. Bahari, N. Hashemzehi, and et al. Association of polymorphisms in glutamate-cysteine ligase catalytic subunit and microsomal triglyceride transfer protein genes with nonalcoholic fatty liver disease DNA Cell Biol 30 2011 569 575
42. A.R. Aroor, J. Habibi, D.A. Ford, R. Nistala, G. Lastra, C. Manrique, and et al. Dipeptidyl peptidase-4 inhibition ameliorates western diet-induced hepatic steatosis and insulin resistance through hepatic lipid remodeling and modulation of hepatic mitochondrial function Diabetes 64 2015 1988 2001
43. A. Chmurzynska Fetal programming: link between early nutrition, DNA methylation, and complex diseases Nutr Rev 68 2010 87 98
44. K. Fujiki, F. Kano, K. Shiota, and M. Murata Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes BMC Biol 7 2009 38
45. X. Chang, H. Yan, J. Fei, M. Jiang, H. Zhu, D. Lu, and et al. Berberine reduces methylation of the MTTP promoter and alleviates fatty liver induced by a high-fat diet in rats J Lipid Res 51 2010 2504 2515
46. Y. Manabe, K.S. Gollisch, L. Holton, Y.B. Kim, J. Brandauer, N.L. Fujii, and et al. Exercise training-induced adaptations associated with increases in skeletal muscle glycogen content FEBS J 280 2013 916 926
47. D.G. Cotter, B. Ercal, X. Huang, J.M. Leid, D.A. d'Avignon, M.J. Graham, and et al. Ketogenesis prevents diet-induced fatty liver injury and hyperglycemia J Clin Invest 124 2014 5175 5190