Hostname: page-component-7c8c6479df-94d59 Total loading time: 0 Render date: 2024-03-28T23:44:25.837Z Has data issue: false hasContentIssue false

MATERNAL OBESITY AND OXIDATIVE STRESS IN THE FETUS: MECHANISMS UNDERLYING EARLY LIFE SHIFTS IN SKELETAL MUSCLE METABOLISM

Published online by Cambridge University Press:  29 July 2011

KRISTEN E BOYLE
Affiliation:
Department of Pediatrics, University of Colorado School of Medicine, Aurora, CO 80045.
JACOB E FRIEDMAN*
Affiliation:
Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Aurora, CO 80045.
*
Jacob E (Jed) Friedman, Department of Pediatrics, University of Colorado School of Medicine, P.O. Box 6511, Mail Stop 8106, Aurora, CO 80045, United States of America E-mail: jed.friedman@ucdenver.edu

Extract

The most common maternal risk factor associated with neonatal complications during delivery is obesity. Although gestational diabetes mellitus (GDM) occurs in 5–10% of the pregnant population, obesity, by virtue of its prevalence, far outpaces GDM as the most important underlying risk factor for increased fetal adiposity. The mechanisms underlying maternal insulin resistance may play an important role in the diversion of excess fuels to the fetus. Maternal adipose depots increase in early pregnancy, followed by increased adipose tissue lipolysis and subsequent hyperlipidaemia, which mainly corresponds to increased triglyceride levels (TG). A positive correlation between maternal TG and infant body weight or fat mass has been found in both GDM and non-GDM obese women. Increased oxidative stress, altered adipokines, and inflammatory cytokines have also been found in obese pregnant women, suggesting an adverse metabolic outcome even in normoglycemic conditions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1Schaefer-Graf, UM, Graf, K, Kulbacka, I, Kjos, SL, Dudenhausen, J, Vetter, K, et al. Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care 2008; 31: 1858–63.CrossRefGoogle ScholarPubMed
2Baird, J, Fisher, D, Lucas, P, Kleijnen, J, Roberts, H, Law, C. Being big or growing fast: systematic review of size and growth in infancy and later obesity. BMJ 2005; 331: 919–20.CrossRefGoogle ScholarPubMed
3Boney, CM, Verma, A, Tucker, R, Vohr, BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005; 115: e2906.CrossRefGoogle ScholarPubMed
4Ouzilleau, C, Roy, MA, Leblanc, L, Carpentier, A, Maheux, P. An observational study comparing 2-hour 75-g oral glucose tolerance with fasting plasma glucose in pregnant women: both poorly predictive of birth weight. CMAJ 2003; 168: 403409.Google ScholarPubMed
5Di Cianni, G, Miccoli, R, Volpe, L, Lencioni, C, Ghio, A, Giovannitti, MG, et al. Maternal triglyceride levels and newborn weight in pregnant women with normal glucose tolerance. Diabet Med 2005; 22: 2125.CrossRefGoogle ScholarPubMed
6Khan, NA. Role of lipids and fatty acids in macrosomic offspring of diabetic pregnancy. Cell Biochem Biophys 2007; 48: 7988.CrossRefGoogle ScholarPubMed
7Weiss, R, Dziura, J, Burgert, TS, Tamborlane, WV, Taksali, SE, Yeckel, CW, et al. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 2004; 350: 2362–374.CrossRefGoogle ScholarPubMed
8Catalano, PM. Pregnancy and lactation in relation to range of acceptable carbohydrate and fat intake. Eur J Clin Nutr 1999; 124–31.CrossRefGoogle Scholar
9Okereke, NC, Huston-Presley, L, Amini, SB, Kalhan, S, Catalano, PM. Longitudinal changes in energy expenditure and body composition in obese women with normal and impaired glucose tolerance. Am J Physiol Endocrinol Metab 2004; 287: E47279.CrossRefGoogle ScholarPubMed
10Challier, JC, Basu, S, Bintein, T, Minium, J, Hotmire, K, Catalano, PM, et al. Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta. Placenta 2008; 29: 274–81.CrossRefGoogle ScholarPubMed
11Madan, JC, Davis, JM, Craig, WY, Collins, M, Allan, W, Quinn, R, et al. Maternal obesity and markers of inflammation in pregnancy. Cytokine 2009; 47: 6164.CrossRefGoogle ScholarPubMed
12Stewart, FM, Freeman, DJ, Ramsay, JE, Greer, IA, Caslake, M, Ferrell, WR. Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers. J Clin Endocrinol Metab 2007; 92: 969–75.CrossRefGoogle Scholar
13Butte, NF, Ellis, KJ, Wong, WW, Hopkinson, JM, Smith, EO. Composition of gestational weight gain impacts maternal fat retention and infant birth weight. Am J Obstet Gynecol 2003; 189: 1423–32.CrossRefGoogle ScholarPubMed
14Lain, KY, Catalano, PM. Metabolic changes in pregnancy. Clin Obstet Gynecol 2007; 50: 938–48.CrossRefGoogle ScholarPubMed
15Villar, J, Cogswell, M, Kestler, E, Castillo, P, Menendez, R, Repke, JT. Effect of fat and fat-free mass deposition during pregnancy on birth weight. Am J Obstet Gynecol 1992; 167: 1344–52.CrossRefGoogle ScholarPubMed
16Alvarez, JJ, Montelongo, A, Iglesias, A, Lasuncion, MA, Herrera, E. Longitudinal study on lipoprotein profile, high density lipoprotein subclass, and postheparin lipases during gestation in women. J Lipid Res 1996; 37: 299308.CrossRefGoogle ScholarPubMed
17Challis, JR, Lockwood, CJ, Myatt, L, Norman, JE, Strauss, JF 3rd, Petraglia, F. Inflammation and pregnancy. Reprod Sci 2009; 16: 206–15.CrossRefGoogle ScholarPubMed
18Schmatz, M, Madan, J, Marino, T, Davis, J. Maternal obesity: the interplay between inflammation, mother and fetus. J Perinatol 2010; 30: 441–46.CrossRefGoogle ScholarPubMed
19Friedman, JE, Kirwan, JP, Jing, M, Presley, L, Catalano, PM. Increased skeletal muscle tumor necrosis factor-alpha and impaired insulin signaling persist in obese women with gestational diabetes mellitus 1 year postpartum. Diabetes 2008; 57: 606–13.CrossRefGoogle ScholarPubMed
20Winkler, G, Cseh, K, Baranyi, E, Melczer, Z, Speer, G, Hajos, P, et al. Tumor necrosis factor system in insulin resistance in gestational diabetes. Diabetes Res Clin Pract 2002; 56: 9399.CrossRefGoogle ScholarPubMed
21Catalano, PM, Nizielski, SE, Shao, J, Preston, L, Qiao, L, Friedman, JE. Downregulated IRS-1 and PPARgamma in obese women with gestational diabetes: relationship to FFA during pregnancy. Am J Physiol Endocrinol Metab 2002; 282: E52233.CrossRefGoogle ScholarPubMed
22Barbour, LA, Shao, J, Qiao, L, Leitner, W, Anderson, M, Friedman, JE, et al. Human placental growth hormone increases expression of the p85 regulatory unit of phosphatidylinositol 3-kinase and triggers severe insulin resistance in skeletal muscle. Endocrinology 2004; 145: 1144–50.CrossRefGoogle ScholarPubMed
23Barbour, LA, Shao, J, Qiao, L, Pulawa, LK, Jensen, DR, Bartke, A, et al. Human placental growth hormone causes severe insulin resistance in transgenic mice. Am J Obstet Gynecol 2002; 186: 512–17.CrossRefGoogle ScholarPubMed
24Kane, DA, Lin, CT, Anderson, EJ, Kwak, HB, Cox, JH, Brophy, PM, et al. Progesterone increases skeletal muscle mitochondrial H2O2 emission in nonmenopausal women. Am J Physiol Endocrinol Metab 2011; 300: E52835.CrossRefGoogle ScholarPubMed
25Livingstone, C, Collison, M. Sex steroids and insulin resistance. Clin Sci 2002; 102: 151–66.CrossRefGoogle ScholarPubMed
26Hauguel-de Mouzon, S, Lepercq, J, Catalano, P. The known and unknown of leptin in pregnancy. Am J Obstet Gynecol 2006; 194: 1537–45.CrossRefGoogle ScholarPubMed
27Catalano, PM, Hoegh, M, Minium, J, Huston-Presley, L, Bernard, S, Kalhan, S, et al. Adiponectin in human pregnancy: implications for regulation of glucose and lipid metabolism. Diabetologia 2006; 49: 1677–85.CrossRefGoogle ScholarPubMed
28Herrera, E. Metabolic adaptations in pregnancy and their implications for the availability of substrates to the fetus. Eur J Clin Nutr 2000; 54 Suppl 1: S4751.CrossRefGoogle ScholarPubMed
29Varastehpour, A, Radaelli, T, Minium, J, Ortega, H, Herrera, E, Catalano, P, et al. Activation of phospholipase A2 is associated with generation of placental lipid signals and fetal obesity. J Clin Endocrinol Metab 2006; 91: 248–55.CrossRefGoogle ScholarPubMed
30Herrera, E, Ortega-Senovilla, H. Disturbances in lipid metabolism in diabetic pregnancy - Are these the cause of the problem? Best Pract Res Clin Endocrinol Metab 2010; 24: 515–25.CrossRefGoogle ScholarPubMed
31Innis, SM. Essential fatty acids in growth and development. Prog Lipid Res 1991; 30: 39103.CrossRefGoogle ScholarPubMed
32Uauy, R, Treen, M, Hoffman, DR. Essential fatty acid metabolism and requirements during development. Semin Perinatol 1989; 13: 118–30.Google ScholarPubMed
33Berggren, JR, Boyle, KE, Chapman, WH, Houmard, JA. Skeletal muscle lipid oxidation and obesity: influence of weight loss and exercise. Am J Physiol Endocrinol Metab 2008; 294: E72632.CrossRefGoogle ScholarPubMed
34Chomentowski, P, Coen, PM, Radikova, Z, Goodpaster, BH, Toledo, FG. Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J Clin Endocrinol Metab 2011; 96: 494503.CrossRefGoogle ScholarPubMed
35He, J, Watkins, S, Kelley, DE. Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 2001; 50: 817–23.CrossRefGoogle ScholarPubMed
36Hulver, MW, Berggren, JR, Carper, MJ, Miyazaki, M, Ntambi, JM, Hoffman, EP, et al. Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty acid partitioning in obese humans. Cell Metab 2005; 2: 251–61.CrossRefGoogle ScholarPubMed
37Hulver, MW, Berggren, JR, Cortright, RN, Dudek, RW, Thompson, RP, Pories, WJ, et al. Skeletal muscle lipid metabolism with obesity. Am J Physiol Endocrinol Metab 2003; 284: E74147.CrossRefGoogle ScholarPubMed
38Kelley, DE, Goodpaster, BH, Storlien, L. Muscle triglyceride and insulin resistance. Annu Rev Nutr 2002; 22: 325–46.CrossRefGoogle ScholarPubMed
39Kelley, DE, He, J, Menshikova, EV, Ritov, VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002; 51: 2944–50.CrossRefGoogle ScholarPubMed
40Kelley, DE, Simoneau, JA. Impaired free fatty acid utilization by skeletal muscle in non-insulin-dependent diabetes mellitus. J Clin Invest 1994; 94: 2349–56.CrossRefGoogle ScholarPubMed
41Kim, JY, Hickner, RC, Cortright, RL, Dohm, GL, Houmard, JA. Lipid oxidation is reduced in obese human skeletal muscle. Am J Physiol Endocrinol Metab 2000; 279: E103944.CrossRefGoogle ScholarPubMed
42Lillioja, S, Young, AA, Culter, CL, Ivy, JL, Abbott, WG, Zawadzki, JK, et al. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 1987; 80: 415–24.CrossRefGoogle ScholarPubMed
43Weisberg, SP, McCann, D, Desai, M, Rosenbaum, M, Leibel, RL, FerranteAW, Jr AW, Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796–808.CrossRefGoogle ScholarPubMed
44Xu, H, Barnes, GT, Yang, Q, Tan, G, Yang, D, Chou, CJ, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821–30.CrossRefGoogle Scholar
45Ehrenberg, HM, Huston-Presley, L, Catalano, PM. The influence of obesity and gestational diabetes mellitus on accretion and the distribution of adipose tissue in pregnancy. Am J Obstet Gynecol 2003; 189: 944–48.CrossRefGoogle ScholarPubMed
46Catalano, PM, Thomas, AJ, Huston, LP, Fung, CM. Effect of maternal metabolism on fetal growth and body composition. Diabetes Care 1998; 21 Suppl 2: B8590.Google ScholarPubMed
47Frias, AE, Morgan, TK, Evans, AE, Rasanen, J, Oh, KY, Thornburg, KL, et al. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology 2011; 152: 2456–64.CrossRefGoogle Scholar
48Lepercq, J, Guerre-Millo, M, Andre, J, Cauzac, M, Hauguel-de Mouzon, S. Leptin: a potential marker of placental insufficiency. Gynecol Obstet Invest 2003; 55: 151–55.CrossRefGoogle ScholarPubMed
49Williams, MA, Qiu, C, Muy-Rivera, M, Vadachkoria, S, Song, T, Luthy, DA. Plasma adiponectin concentrations in early pregnancy and subsequent risk of gestational diabetes mellitus. J Clin Endocrinol Metab 2004; 89: 2306–11.CrossRefGoogle ScholarPubMed
50Magnusson-Olsson, AL, Hamark, B, Ericsson, A, Wennergren, M, Jansson, T, Powell, TL. Gestational and hormonal regulation of human placental lipoprotein lipase. J Lipid Res 2006; 47: 2551–61.CrossRefGoogle ScholarPubMed
51Marseille-Tremblay, C, Ethier-Chiasson, M, Forest, JC, Giguere, Y, Masse, A, Mounier, C, et al. Impact of maternal circulating cholesterol and gestational diabetes mellitus on lipid metabolism in human term placenta. Mol Reprod Dev 2008; 75: 1054–62.CrossRefGoogle ScholarPubMed
52Zhu, MJ, Du, M, Nathanielsz, PW, Ford, SP. Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta. Placenta 2010; 31: 387–91.CrossRefGoogle ScholarPubMed
53Heerwagen, MJ, Miller, MR, Barbour, LA, Friedman, JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Physiol Regul Integr Comp Physiol 2010; 299: R71122.CrossRefGoogle ScholarPubMed
54Du, M, Yan, X, Tong, JF, Zhao, J, Zhu, MJ. Maternal obesity, inflammation, and fetal skeletal muscle development. Biol Reprod 2010; 82: 412.CrossRefGoogle ScholarPubMed
55Igosheva, N, Abramov, AY, Poston, L, Eckert, JJ, Fleming, TP, Duchen, MR, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 2010; 5: e10074.CrossRefGoogle ScholarPubMed
56Iyer, NV, Kotch, LE, Agani, F, Leung, SW, Laughner, E, Wenger, RH, et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 1998; 12: 149–62.CrossRefGoogle ScholarPubMed
57Ryan, HE, Lo, J, Johnson, RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J 1998; 17: 3005–15.CrossRefGoogle ScholarPubMed
58Jarvie, E, Hauguel-de-Mouzon, S, Nelson, SM, Sattar, N, Catalano, PM, Freeman, DJ. Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring. Clin Sci 2010; 119: 123–29.CrossRefGoogle ScholarPubMed
59Lopez-Tinoco, C, Roca, M, Garcia-Valero, A, Murri, M, Tinahones, FJ, Segundo, C, et al. Oxidative stress and antioxidant status in patients with late-onset gestational diabetes mellitus. Acta Diabetol 2011; Feb 17, epub ahead of print.CrossRefGoogle Scholar
60McCurdy, CE, Bishop, JM, Williams, SM, Grayson, BE, Smith, MS, Friedman, JE, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest 2009; 119: 323–35.Google ScholarPubMed
61Bouanane, S, Benkalfat, NB, Baba Ahmed, FZ, Merzouk, H, Mokhtari, NS, Merzouk, SA, et al. Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring. Clin Sci 2009; 116: 669–80.CrossRefGoogle ScholarPubMed
62Catalano, PM, Presley, L, Minium, J, Hauguel-de Mouzon, S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 2009; 32: 1076–80.CrossRefGoogle ScholarPubMed
63Chiavaroli, V, Giannini, C, D'Adamo, E, de Giorgis, T, Chiarelli, F, Mohn, A. Insulin resistance and oxidative stress in children born small and large for gestational age. Pediatrics 2009; 124: 695702.CrossRefGoogle ScholarPubMed
64Freeman, DJ. Effects of maternal obesity on fetal growth and body composition: implications for programming and future health. Semin Fetal Neonatal Med 2010; 15: 113188.CrossRefGoogle ScholarPubMed
65Tong, JF, Yan, X, Zhu, MJ, Ford, SP, Nathanielsz, PW, Du, M. Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle. Am J Physiol Endocrinol Metab 2009; 296: E91724.CrossRefGoogle ScholarPubMed
66Yan, X, Zhu, MJ, Xu, W, Tong, JF, Ford, SP, Nathanielsz, PW, et al. Up-regulation of Toll-like receptor 4/nuclear factor-kappaB signaling is associated with enhanced adipogenesis and insulin resistance in fetal skeletal muscle of obese sheep at late gestation. Endocrinology 2010; 151: 380–87.CrossRefGoogle ScholarPubMed
67Zhu, MJ, Han, B, Tong, J, Ma, C, Kimzey, JM, Underwood, KR, et al. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J Physiol 2008; 586: 2651–64.CrossRefGoogle ScholarPubMed
68Catalano, PM, Ehrenberg, HM. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG 2006; 113: 1126–33.CrossRefGoogle Scholar
69Sanchez-Vera, I, Bonet, B, Viana, M, Quintanar, A, Martin, MD, Blanco, P, et al. Changes in plasma lipids and increased low-density lipoprotein susceptibility to oxidation in pregnancies complicated by gestational diabetes: consequences of obesity. Metabolism 2007; 56: 1527–33.CrossRefGoogle ScholarPubMed
70Allen, RG. Oxygen-reactive species and antioxidant responses during development: the metabolic paradox of cellular differentiation. Proc Soc Exp Biol Med 1991; 196: 117–29.CrossRefGoogle ScholarPubMed
71Jezek, P, Hlavata, L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int J Biochem Cell Biol 2005; 37: 2478–503.CrossRefGoogle ScholarPubMed
72McClintock, DS, Santore, MT, Lee, VY, Brunelle, J, Budinger, GR, Zong, WX, et al. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol Cell Biol 2002; 22: 94104.CrossRefGoogle ScholarPubMed
73Fabbrini, E, Magkos, F, Mohammed, BS, Pietka, T, Abumrad, NA, Patterson, BW, et al. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci USA 2009; 106: 15430–35.CrossRefGoogle Scholar
74Goodpaster, BH, Theriault, R, Watkins, SC, Kelley, DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000; 49: 467–72.CrossRefGoogle ScholarPubMed
75Stefan, N, Kantartzis, K, Machann, J, Schick, F, Thamer, C, Rittig, K, et al. Identification and characterization of metabolically benign obesity in humans. Arch Intern Med 2008; 168: 1609–16.CrossRefGoogle ScholarPubMed
76van Herpen, NA, Schrauwen-Hinderling, VB. Lipid accumulation in non-adipose tissue and lipotoxicity. Physiol Behav 2008; 94: 231–41.CrossRefGoogle ScholarPubMed
77Schrauwen, P. High-fat diet, muscular lipotoxicity and insulin resistance. Proc Nutr Soc 2007; 66: 3341.CrossRefGoogle ScholarPubMed
78Reyna, SM, Ghosh, S, Tantiwong, P, Meka, CS, Eagan, P, Jenkinson, CP, et al. Elevated toll-like receptor 4 expression and signaling in muscle from insulin-resistant subjects. Diabetes 2008; 57: 2595–602.CrossRefGoogle ScholarPubMed
79Schaeffler, A, Gross, P, Buettner, R, Bollheimer, C, Buechler, C, Neumeier, M, et al. Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology 2009; 126: 233–45.CrossRefGoogle ScholarPubMed
80Sen, S, Simmons, RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes 2010; 59: 3058–65.CrossRefGoogle ScholarPubMed
81Davis, JM, Auten, RL. Maturation of the antioxidant system and the effects on preterm birth. Semin Fetal Neonatal Med 2010; 15: 191–95.CrossRefGoogle ScholarPubMed
82Fantel, AG, Mackler, B, Stamps, LD, Tran, TT, Person, RE. Reactive oxygen species and DNA oxidation in fetal rat tissues. Free Radic Biol Med 1998; 25: 95103.CrossRefGoogle ScholarPubMed
83Qanungo, S, Mukherjea, M. Ontogenic profile of some antioxidants and lipid peroxidation in human placental and fetal tissues. Mol Cell Biochem 2000; 215: 1119.CrossRefGoogle ScholarPubMed
84Mackler, B, Person, RE, Nguyen, TD, Fantel, AG. Studies of the cellular distribution of superoxide dismutases in adult and fetal rat tissues. Free Radic Res 1998; 28: 125–29.CrossRefGoogle ScholarPubMed
85Mover, H, Ar, A. Antioxidant enzymatic activity in embryos and placenta of rats chronically exposed to hypoxia and hyperoxia. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1997; 117: 151–57.CrossRefGoogle ScholarPubMed
86Brauner, P, Kopecky, P, Flachs, P, Ruffer, J, Sebron, V, Plavka, R, et al. Induction of uncoupling protein 3 gene expression in skeletal muscle of preterm newborns. Pediatr Res 2003; 53: 691–97.CrossRefGoogle ScholarPubMed
87Bogavac, M, Lakic, N, Simin, N, Nikolic, A, Sudji, J, Bozin, B. Biomarkers of oxidative stress in amniotic fluid and complications in pregnancy. J Matern Fetal Neonatal Med 2011; Mar 10, epub ahead of print.CrossRefGoogle Scholar
88Giugliano, D, Ceriello, A, Paolisso, G. Oxidative stress and diabetic vascular complications. Diabetes Care 1996; 19: 257–67.CrossRefGoogle ScholarPubMed
89Patil, SB, Kodliwadmath, MV, Kodliwadmath, M. Lipid peroxidation and antioxidant activity in complicated pregnancies. Clin Exp Obstet Gynecol 2009; 36: 110–12.Google ScholarPubMed
90Wang, Y, Walsh, SW. Increased superoxide generation is associated with decreased superoxide dismutase activity and mRNA expression in placental trophoblast cells in pre-eclampsia. Placenta 2001; 22: 206–12.CrossRefGoogle ScholarPubMed
91Wisdom, SJ, Wilson, R, McKillop, JH, Walker, JJ. Antioxidant systems in normal pregnancy and in pregnancy-induced hypertension. Am J Obstet Gynecol 1991; 165: 1701–704.CrossRefGoogle ScholarPubMed
92Al-Saleh, E, Nandakumaran, M, Al-Harmi, J, Sadan, T, Al-Enezi, H. Maternal-fetal status of copper, iron, molybdenum, selenium, and zinc in obese pregnant women in late gestation. Biol Trace Elem Res 2006; 113: 113–23.CrossRefGoogle ScholarPubMed
93Al-Saleh, E, Nandakumaran, M, Al-Rashdan, I, Al-Harmi, J, Al-Shammari, M. Maternal-foetal status of copper, iron, molybdenum, selenium and zinc in obese gestational diabetic pregnancies. Acta Diabetol 2007; 44: 106–13.CrossRefGoogle ScholarPubMed
94Cox, J, Williams, S, Grove, K, Lane, RH, Aagaard-Tillery, KM. A maternal high-fat diet is accompanied by alterations in the fetal primate metabolome. Am J Obstet Gynecol 2009; 201: 281 e19.CrossRefGoogle ScholarPubMed
95Chappell, LC, Seed, PT, Briley, AL, Kelly, FJ, Lee, R, Hunt, BJ, et al. Effect of antioxidants on the occurrence of pre-eclampsia in women at increased risk: a randomised trial. Lancet 1999; 354: 810–16.CrossRefGoogle Scholar
96Roberts, JM, Myatt, L, Spong, CY, Thom, EA, Hauth, JC, Leveno, KJ, et al. Vitamins C and E to prevent complications of pregnancy-associated hypertension. N Engl J Med 2010; 362: 1282–91.CrossRefGoogle Scholar
97Basaran, A, Basaran, M, Topatan, B. Combined vitamin C and E supplementation for the prevention of preeclampsia: a systematic review and meta-analysis. Obstet Gynecol Surv 2010; 65: 653–67.CrossRefGoogle Scholar
98Poston, L, Briley, AL, Seed, PT, Kelly, FJ, Shennan, AH. Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial. Lancet 2006; 367: 1145–54.CrossRefGoogle ScholarPubMed
99Barbet, JP, Thornell, LE, Butler-Browne, GS. Immunocytochemical characterisation of two generations of fibers during the development of the human quadriceps muscle. Mech Dev 1991; 35: 311.CrossRefGoogle ScholarPubMed
100Pin, CL, Hrycyshyn, AW, Rogers, KA, Rushlow, WJ, Merrifield, PA. Embryonic and fetal rat myoblasts form different muscle fiber types in an ectopic in vivo environment. Dev Dyn 2002; 224: 253–66.CrossRefGoogle Scholar
101Van Swearingen, J, Lance-Jones, C. Slow and fast muscle fibers are preferentially derived from myoblasts migrating into the chick limb bud at different developmental times. Dev Biol 1995 Aug; 170: 321–37.CrossRefGoogle ScholarPubMed
102Ross, JJ, Duxson, MJ, Harris, AJ. Neural determination of muscle fibre numbers in embryonic rat lumbrical muscles. Development 1987; 100: 395409.CrossRefGoogle ScholarPubMed
103Stockdale, FE. Myogenic cell lineages. Dev Biol 1992; 154: 284–98.CrossRefGoogle ScholarPubMed
104Torgan, CE, Daniels, MP. Regulation of myosin heavy chain expression during rat skeletal muscle development in vitro. Mol Biol Cell 2001; 12: 1499–508.CrossRefGoogle ScholarPubMed
105Dauncey, MJ, Gilmour, RS. Regulatory factors in the control of muscle development. Proc Nutr Soc 1996; 55: 543–59.CrossRefGoogle ScholarPubMed
106Edom-Vovard, F, Mouly, V, Barbet, JP, Butler-Browne, GS. The four populations of myoblasts involved in human limb muscle formation are present from the onset of primary myotube formation. J Cell Sci 1999; 112: 191–99.CrossRefGoogle ScholarPubMed
107Warhol, MJ, Siegel, AJ, Evans, WJ, Silverman, LM. Skeletal muscle injury and repair in marathon runners after competition. Am J Pathol 1985; 118: 331–39.Google ScholarPubMed
108Bell, JA, Reed, MA, Consitt, LA, Martin, OJ, Haynie, KR, Hulver, MW, et al. Lipid partitioning, incomplete fatty acid oxidation, and insulin signal transduction in primary human muscle cells: effects of severe obesity, fatty acid incubation, and fatty acid translocase/CD36 overexpression. J Clin Endocrinol Metab 2010; 95: 3400–10.CrossRefGoogle ScholarPubMed
109Berggren, JR, Tanner, CJ, Houmard, JA. Primary cell cultures in the study of human muscle metabolism. Exerc Sport Sci Rev 2007; 35: 5661.CrossRefGoogle Scholar
110Consitt, LA, Bell, JA, Koves, TR, Muoio, DM, Hulver, MW, Haynie, KR, et al. Peroxisome proliferator-activated receptor-gamma coactivator-1alpha overexpression increases lipid oxidation in myocytes from extremely obese individuals. Diabetes 2010; 59: 1407–15.CrossRefGoogle ScholarPubMed
111Gaster, M. Reduced lipid oxidation in myotubes established from obese and type 2 diabetic subjects. Biochem Biophys Res Commun 2009; 382: 766–70.CrossRefGoogle ScholarPubMed
112Gaster, M, Petersen, I, Hojlund, K, Poulsen, P, Beck-Nielsen, H. The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity. Diabetes 2002; 51: 921–27.CrossRefGoogle ScholarPubMed
113Hittel, DS, Berggren, JR, Shearer, J, Boyle, K, Houmard, JA. Increased secretion and expression of myostatin in skeletal muscle from extremely obese women. Diabetes 2009; 58: 3038.CrossRefGoogle ScholarPubMed
114Ukropcova, B, McNeil, M, Sereda, O, de Jonge, L, Xie, H, Bray, GA, et al. Dynamic changes in fat oxidation in human primary myocytes mirror metabolic characteristics of the donor. J Clin Invest 2005; 115: 1934–41.CrossRefGoogle ScholarPubMed
115Liu, X, Rubin, JS, Kimmel, AR. Rapid, Wnt-induced changes in GSK3beta associations that regulate beta-catenin stabilization are mediated by Galpha proteins. Curr Biol 2005; 15: 1989–97.CrossRefGoogle ScholarPubMed
116Cserjesi, P, Olson, EN. Myogenin induces the myocyte-specific enhancer binding factor MEF-2 independently of other muscle-specific gene products. Mol Cell Biol 1991; 11: 4854–62.Google ScholarPubMed
117Potthoff, MJ, Olson, EN. MEF2: a central regulator of diverse developmental programs. Development 2007; 134: 4131–40.CrossRefGoogle ScholarPubMed
118Zhu, MJ, Ford, SP, Nathanielsz, PW, Du, M. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol Reprod 2004; 71: 1968–73.CrossRefGoogle ScholarPubMed
119Desai, M, Crowther, NJ, Lucas, A, Hales, CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 1996; 76: 591603.CrossRefGoogle ScholarPubMed
120Maltin, CA. Muscle development and obesity: Is there a relationship? Organogenesis 2008; 4: 158–69.CrossRefGoogle ScholarPubMed
121Essen, B, Jansson, E, Henriksson, J, Taylor, AW, Saltin, B. Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiol Scand 1975; 95: 153–65.CrossRefGoogle ScholarPubMed
122Gregory, CM, Vandenborne, K, Dudley, GA. Metabolic enzymes and phenotypic expression among human locomotor muscles. Muscle Nerve 2001; 24: 387–93.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
123James, DE, Jenkins, AB, Kraegen, EW. Heterogeneity of insulin action in individual muscles in vivo: euglycemic clamp studies in rats. Am J Physiol 1985; 248: E56774.Google ScholarPubMed
124Pette, D, Staron, RS. Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 1990; 116: 176.Google ScholarPubMed
125Simoneau, JA, Bouchard, C. Genetic determinism of fiber type proportion in human skeletal muscle. FASEB J 1995; 9: 1091–95.CrossRefGoogle ScholarPubMed
126Chang, JH, Lin, KH, Shih, CH, Chang, YJ, Chi, HC, Chen, SL. Myogenic basic helix-loop-helix proteins regulate the expression of peroxisomal proliferator activated receptor-gamma coactivator-1alpha. Endocrinology 2006; 147: 3093–106.CrossRefGoogle ScholarPubMed
127Czubryt, MP, McAnally, J, Fishman, GI, Olson, EN. Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci USA. 2003; 100: 1711–6.CrossRefGoogle ScholarPubMed
128Lin, J, Wu, H, Tarr, PT, Zhang, CY, Wu, Z, Boss, O, et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418: 797801.CrossRefGoogle ScholarPubMed
129Mortensen, OH, Frandsen, L, Schjerling, P, Nishimura, E, Grunnet, N. PGC-1alpha and PGC-1beta have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am J Physiol Endocrinol Metab 2006; 291: E80716.CrossRefGoogle ScholarPubMed
130DiMario, JX. Protein kinase C signaling controls skeletal muscle fiber types. Exp Cell Res 2001; 263: 2332.CrossRefGoogle ScholarPubMed
131DiMario, JX, Funk, PE. Protein kinase C activity regulates slow myosin heavy chain 2 gene expression in slow lineage skeletal muscle fibers. Dev Dyn 1999; 216: 177–89.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
132Hickey, MS, Carey, JO, Azevedo, JL, Houmard, JA, Pories, WJ, Israel, RG, et al. Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 1995; 268: E45357.Google ScholarPubMed
133Marin, P, Andersson, B, Krotkiewski, M, Bjorntorp, P. Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 1994; 17: 382–86.CrossRefGoogle ScholarPubMed
134Oberbach, A, Bossenz, Y, Lehmann, S, Niebauer, J, Adams, V, Paschke, R, et al. Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 2006; 29: 895900.CrossRefGoogle ScholarPubMed
135Tanner, CJ, Barakat, HA, Dohm, GL, Pories, WJ, MacDonald, KG, Cunningham, PR, et al. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 2002; 282: E119196.CrossRefGoogle ScholarPubMed
136Malenfant, P, Joanisse, DR, Theriault, R, Goodpaster, BH, Kelley, DE, Simoneau, JA. Fat content in individual muscle fibers of lean and obese subjects. Int J Obes Relat Metab Disord 2001; 25: 1316–321.CrossRefGoogle ScholarPubMed
137Gerrits, MF, Ghosh, S, Kavaslar, N, Hill, B, Tour, A, Seifert, EL, et al. Distinct skeletal muscle fiber characteristics and gene expression in diet-sensitive versus diet-resistant obesity. J Lipid Res 2010; 51: 2394–404.CrossRefGoogle ScholarPubMed
138Conley, KE, Amara, CE, Jubrias, SA, Marcinek, DJ. Mitochondrial function, fibre types and ageing: new insights from human muscle in vivo. Exp Physiol 2007; 92: 333–39.CrossRefGoogle ScholarPubMed
139Harper, ME, Dent, R, Monemdjou, S, Bezaire, V, Van Wyck, L, Wells, G, et al. Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes 2002; 51: 2459–466.CrossRefGoogle ScholarPubMed
140Wensaas, AJ, Rustan, AC, Just, M, Berge, RK, Drevon, CA, Gaster, M. Fatty acid incubation of myotubes from humans with type 2 diabetes leads to enhanced release of beta-oxidation products because of impaired fatty acid oxidation: effects of tetradecylthioacetic acid and eicosapentaenoic acid. Diabetes 2009; 58: 527–35.CrossRefGoogle ScholarPubMed
141Berggren, JR, Hulver, MW, Dohm, GL, Houmard, JA. Weight loss and exercise: implications for muscle lipid metabolism and insulin action. Med Sci Sports Exerc 2004; 36: 1191–195.CrossRefGoogle ScholarPubMed
142Kelley, DE, Goodpaster, B, Wing, RR, Simoneau, JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999; 277: E113041.Google ScholarPubMed
143Koves, TR, Ussher, JR, Noland, RC, Slentz, D, Mosedale, M, Ilkayeva, O, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 2008; 7: 4556.CrossRefGoogle ScholarPubMed
144Astrup, A, Buemann, B, Christensen, NJ, Toubro, S. Failure to increase lipid oxidation in response to increasing dietary fat content in formerly obese women. Am J Physiol 1994; 266: E59299.Google ScholarPubMed
145Boyle, KE, Canham, JP, Consitt, LA, Zheng, D, Koves, TR, Gavin, TP, et al. A high-fat diet elicits differential responses in genes coordinating oxidative metabolism in skeletal muscle of lean and obese individuals. J Clin Endocrinol Metab 2011; 96: 775–81.CrossRefGoogle ScholarPubMed
146Schrauwen, P, van Marken Lichtenbelt, WD, Saris, WH, Westerterp, KR. Changes in fat oxidation in response to a high-fat diet. Am J Clin Nutr 1997; 66: 276–82.CrossRefGoogle ScholarPubMed
147Schrauwen, P, van Marken Lichtenbelt, WD, Westerterp, KR. Fat and carbohydrate balances during adaptation to a high-fat diet. Am J Clin Nutr 2000; 72: 1239–41.CrossRefGoogle ScholarPubMed
148Smith, SR, de Jonge, L, Zachwieja, JJ, Roy, H, Nguyen, T, Rood, JC, et al. Fat and carbohydrate balances during adaptation to a high-fat. Am J Clin Nutr 2000; 71: 450–57.CrossRefGoogle ScholarPubMed
149Thomas, CD, Peters, JC, Reed, GW, Abumrad, NN, Sun, M, Hill, JO. Nutrient balance and energy expenditure during ad libitum feeding of high-fat and high-carbohydrate diets in humans. Am J Clin Nutr 1992; 55: 934–42.CrossRefGoogle ScholarPubMed
150Steinberg, GR, Michell, BJ, van Denderen, BJ, Watt, MJ, Carey, AL, Fam, BC, et al. Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 2006; 4: 465–74.CrossRefGoogle ScholarPubMed
151Dabelea, D, Dolan, LM, D'AgostinoR, Jr. R, Jr., Hernandez, AM, McAteer, JB, Hamman, RF, et al. Association testing of TCF7L2 polymorphisms with type 2 diabetes in multi-ethnic youth. Diabetologia 2011; 54: 535–39.CrossRefGoogle ScholarPubMed
152Bayol, SA, Simbi, BH, Stickland, NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 2005; 567: 951–61.CrossRefGoogle ScholarPubMed
153Shelley, P, Martin-Gronert, MS, Rowlerson, A, Poston, L, Heales, SJ, Hargreaves, IP, et al. Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice. Am J Physiol Regul Integr Comp Physiol 2009; 297: R67581.CrossRefGoogle ScholarPubMed
154Simar, D, Chen, H, Lambert, K, Mercier, J, Morris, MJ. Interaction between maternal obesity and post-natal over-nutrition on skeletal muscle metabolism. Nutr Metab Cardiovasc Dis 2011; Jan 3, epub ahead of print.CrossRefGoogle Scholar
155He, D, Bolstad, G, Brubakk, A, Medbo, JI. Muscle fibre type and dimension in genetically obese and lean Zucker rats. Acta Physiol Scand 1995; 155: 17.CrossRefGoogle ScholarPubMed
156Kemp, JG, Blazev, R, Stephenson, DG, Stephenson, GM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 2009; 33: 831–41.CrossRefGoogle ScholarPubMed
157Paturi, S, Gutta, AK, Kakarla, SK, Katta, A, Arnold, EC, Wu, M, et al. Impaired overload-induced hypertrophy in obese Zucker rat slow-twitch skeletal muscle. J Appl Physiol 2010; 108: 713.CrossRefGoogle ScholarPubMed
158Pescatello, LS, Kelsey, BK, Price, TB, Seip, RL, Angelopoulos, TJ, Clarkson, PM, et al. The muscle strength and size response to upper arm, unilateral resistance training among adults who are overweight and obese. J Strength Cond Res 2007; 21: 307–13.Google ScholarPubMed
159Lattuada, G, Costantino, F, Caumo, A, Scifo, P, Ragogna, F, De Cobelli, F, et al. Reduced whole-body lipid oxidation is associated with insulin resistance, but not with intramyocellular lipid content in offspring of type 2 diabetic patients. Diabetologia 2005; 48: 741–47.CrossRefGoogle Scholar
160Perseghin, G, Scifo, P, De Cobelli, F, Pagliato, E, Battezzati, A, Arcelloni, C, et al. Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 1999; 48: 1600–606.CrossRefGoogle ScholarPubMed
161Jauniaux, E, Watson, A, Burton, G. Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks’ gestation. Am J Obstet Gynecol 2001; 184: 9981003.CrossRefGoogle ScholarPubMed
162Land, SC. Oxygen-sensing pathways and the development of mammalian gas exchange. Redox Rep 2003; 8: 325–40.CrossRefGoogle ScholarPubMed
163Buonocore, G, Perrone, S, Tataranno, ML. Oxygen toxicity: chemistry and biology of reactive oxygen species. Semin Fetal Neonatal Med 2010; 15: 186–90.CrossRefGoogle ScholarPubMed
164Fischer, B, Bavister, BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil 1993; 99: 673–79.CrossRefGoogle ScholarPubMed
165Adelman, DM, Gertsenstein, M, Nagy, A, Simon, MC, Maltepe, E. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 2000; 14: 3191–203.CrossRefGoogle ScholarPubMed
166Cowden Dahl, KD, Fryer, BH, Mack, FA, Compernolle, V, Maltepe, E, Adelman, DM, et al. Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol 2005; 25: 10479–91.CrossRefGoogle ScholarPubMed
167Fryer, BH, Simon, MC. Hypoxia, HIF and the placenta. Cell Cycle 2006; 5: 495–98.CrossRefGoogle ScholarPubMed
168Maltepe, E, Krampitz, GW, Okazaki, KM, Red-Horse, K, Mak, W, Simon, MC, et al. Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 2005; 132: 3393–403.CrossRefGoogle ScholarPubMed
169Semenza, GL, Wang, GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992; 12: 5447–54.Google Scholar
170Bell, EL, Chandel, NS. Mitochondrial oxygen sensing: regulation of hypoxia-inducible factor by mitochondrial generated reactive oxygen species. Essays Biochem 2007; 43: 1727.Google ScholarPubMed
171Bell, EL, Klimova, TA, Eisenbart, J, Moraes, CT, Murphy, MP, Budinger, GR, et al. The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 2007; 177: 1029–36.CrossRefGoogle ScholarPubMed
172Chandel, NS. Mitochondrial regulation of oxygen sensing. Adv Exp Med Biol 2010; 661: 339–54.CrossRefGoogle ScholarPubMed
173Chandel, NS, McClintock, DS, Feliciano, CE, Wood, TM, Melendez, JA, Rodriguez, AM, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000; 275: 25130–138.CrossRefGoogle ScholarPubMed
174Hewitson, KS, Lienard, BM, McDonough, MA, Clifton, IJ, Butler, D, Soares, AS, et al. Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J Biol Chem 2007; 282: 3293–301.CrossRefGoogle ScholarPubMed
175Koivunen, P, Hirsila, M, Remes, AM, Hassinen, IE, Kivirikko, KI, Myllyharju, J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 2007; 282: 4524–532.CrossRefGoogle ScholarPubMed
176Page, EL, Chan, DA, Giaccia, AJ, Levine, M, Richard, DE. Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol Cell 2008; 19: 8694.CrossRefGoogle ScholarPubMed
177Semenza, GL. Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007 Oct 9; 2007(407):cm8.CrossRefGoogle Scholar
178Liu, Y, Cox, SR, Morita, T, Kourembanas, S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5’ enhancer. Circ Res 1995; 77: 638–43.CrossRefGoogle ScholarPubMed
179Caniggia, I, Winter, JL. Adriana and Luisa Castellucci Award lecture 2001. Hypoxia inducible factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies–a review. Placenta 2002; 23 Suppl A: S4757.CrossRefGoogle ScholarPubMed
180Rajakumar, A, Brandon, HM, Daftary, A, Ness, R, Conrad, KP. Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Placenta 2004; 25: 763–69.CrossRefGoogle ScholarPubMed
181Rolfo, A, Many, A, Racano, A, Tal, R, Tagliaferro, A, Ietta, F, et al. Abnormalities in oxygen sensing define early and late onset preeclampsia as distinct pathologies. PLoS One 2010; 5: e13288.CrossRefGoogle ScholarPubMed
182Liao, SY, Lerman, MI, Stanbridge, EJ. Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development. BMC Dev Biol 2009; 9: 22.CrossRefGoogle ScholarPubMed
183Kurihara, T, Kubota, Y, Ozawa, Y, Takubo, K, Noda, K, Simon, MC, et al. von Hippel-Lindau protein regulates transition from the fetal to the adult circulatory system in retina. Development 2010; 137: 1563–571.CrossRefGoogle Scholar
184Madan, A, Varma, S, Cohen, HJ. Developmental stage-specific expression of the alpha and beta subunits of the HIF-1 protein in the mouse and human fetus. Mol Genet Metab 2002; 75b: 244–49.CrossRefGoogle ScholarPubMed
185Nau, PN, Van Natta, T, Ralphe, JC, Teneyck, CJ, Bedell, KA, Caldarone, CA, et al. Metabolic adaptation of the fetal and postnatal ovine heart: regulatory role of hypoxia-inducible factors and nuclear respiratory factor-1. Pediatr Res 2002; 52: 269–78.CrossRefGoogle ScholarPubMed
186Firth, JD, Ebert, BL, Pugh, CW, Ratcliffe, PJ. Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3’ enhancer. Proc Natl Acad Sci USA. 1994; 91: 6496–500.CrossRefGoogle ScholarPubMed
187Kim, JW, Tchernyshyov, I, Semenza, GL, Dang, CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006; 3: 177–85.CrossRefGoogle ScholarPubMed
188Seagroves, TN, Ryan, HE, Lu, H, Wouters, BG, Knapp, M, Thibault, P, et al. Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol Cell Biol 2001; 21: 3436–444.CrossRefGoogle ScholarPubMed
189Weidemann, A, Johnson, RS. Biology of HIF-1alpha. Cell Death Differ 2008; 15: 621–27.CrossRefGoogle ScholarPubMed
190Minai, L, Martinovic, J, Chretien, D, Dumez, F, Razavi, F, Munnich, A, et al. Mitochondrial respiratory chain complex assembly and function during human fetal development. Mol Genet Metab 2008; 94: 120–26.CrossRefGoogle ScholarPubMed
191Pejznochova, M, Tesarova, M, Hansikova, H, Magner, M, Honzik, T, Vinsova, K, et al. Mitochondrial DNA content and expression of genes involved in mtDNA transcription, regulation and maintenance during human fetal development. Mitochondrion 2010; 10: 321–29.CrossRefGoogle ScholarPubMed
192Sperl, W, Sengers, RC, Trijbels, JM, Ruitenbeek, W, Doesburg, WH, Smeitink, JA, et al. Enzyme activities of the mitochondrial energy generating system in skeletal muscle tissue of preterm and fullterm neonates. Ann Clin Biochem 1992; 29: 638–45.CrossRefGoogle ScholarPubMed
193Peltzer, J, Carpentier, G, Martelly, I, Courty, J, Keller, A. Transitions towards either slow-oxidative or fast-glycolytic phenotype can be induced in the murine WTt myogenic cell line. J Cell Biochem 2010; 111: 8293.CrossRefGoogle ScholarPubMed
194Ahmetov, II, Hakimullina, AM, Lyubaeva, EV, Vinogradova, OL, Rogozkin, VA. Effect of HIF1A gene polymorphism on human muscle performance. Bull Exp Biol Med 2008; 146: 351–53.CrossRefGoogle ScholarPubMed
195Echtay, KS, Esteves, TC, Pakay, JL, Jekabsons, MB, Lambert, AJ, Portero-Otin, M, et al. A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J 2003; 22: 4103–110.CrossRefGoogle ScholarPubMed
196Murray, AJ, Panagia, M, Hauton, D, Gibbons, GF, Clarke, K. Plasma free fatty acids and peroxisome proliferator-activated receptor alpha in the control of myocardial uncoupling protein levels. Diabetes 2005; 54: 3496–502.CrossRefGoogle ScholarPubMed
197Anderson, EJ, Lustig, ME, Boyle, KE, Woodlief, TL, Kane, DA, Lin, CT, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009; 119: 573–81.CrossRefGoogle Scholar
198Nabben, M, Hoeks, J, Briede, JJ, Glatz, JF, Moonen-Kornips, E, Hesselink, MK, et al. The effect of UCP3 overexpression on mitochondrial ROS production in skeletal muscle of young versus aged mice. FEBS Lett 2008; 582: 4147–152.CrossRefGoogle ScholarPubMed
199Schrauwen, P, Schrauwen-Hinderling, V, Hoeks, J, Hesselink, MK. Mitochondrial dysfunction and lipotoxicity. Biochim Biophys Acta 2010; 1801: 266–71.CrossRefGoogle ScholarPubMed
200Byrne, K, Vuocolo, T, Gondro, C, White, JD, Cockett, NE, Hadfield, T, et al. A gene network switch enhances the oxidative capacity of ovine skeletal muscle during late fetal development. BMC Genomics 2010; 11: 378.CrossRefGoogle ScholarPubMed
201Aucouturier, J, Duche, P, Timmons, BW. Metabolic flexibility and obesity in children and youth. Obes Rev 2010; Oct 26.CrossRefGoogle Scholar
202Kelley, DE, Mandarino, LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 2000; 49: 677–83.CrossRefGoogle ScholarPubMed
203Perseghin, G, Bonfanti, R, Magni, S, Lattuada, G, De Cobelli, F, Canu, T, et al. Insulin resistance and whole body energy homeostasis in obese adolescents with fatty liver disease. Am J Physiol Endocrinol Metab 2006; 291: E697703.CrossRefGoogle ScholarPubMed
204Heilbronn, LK, Gregersen, S, Shirkhedkar, D, Hu, D, Campbell, LV. Impaired fat oxidation after a single high-fat meal in insulin-sensitive nondiabetic individuals with a family history of type 2 diabetes. Diabetes 2007; 56: 2046–53.CrossRefGoogle ScholarPubMed
205Lillycrop, KA, Phillips, ES, Jackson, AA, Hanson, MA, Burdge, GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005; 135: 1382–386.CrossRefGoogle ScholarPubMed
206Barres, R, Osler, ME, Yan, J, Rune, A, Fritz, T, Caidahl, K, et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009; 10: 189–98.CrossRefGoogle ScholarPubMed
207Winder, WW, Wilson, HA, Hardie, DG, Rasmussen, BB, Hutber, CA, Call, GB, et al. Phosphorylation of rat muscle acetyl-CoA carboxylase by AMP-activated protein kinase and protein kinase A. J Appl Physiol 1997; 82: 219–25.CrossRefGoogle ScholarPubMed
208Zong, H, Ren, JM, Young, LH, Pypaert, M, Mu, J, Birnbaum, MJ, et al. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA. 2002; 99: 15983–987.CrossRefGoogle ScholarPubMed
209Long, YC, Barnes, BR, Mahlapuu, M, Steiler, TL, Martinsson, S, Leng, Y, et al. Role of AMP-activated protein kinase in the coordinated expression of genes controlling glucose and lipid metabolism in mouse white skeletal muscle. Diabetologia 2005; 48: 2354–364.CrossRefGoogle ScholarPubMed
210Hardie, DG. Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism. Proc Nutr Soc 2011; 70: 9299.CrossRefGoogle ScholarPubMed
211Hojlund, K, Mustard, KJ, Staehr, P, Hardie, DG, Beck-Nielsen, H, Richter, EA, et al. AMPK activity and isoform protein expression are similar in muscle of obese subjects with and without type 2 diabetes. Am J Physiol Endocrinol Metab 2004; 286: E23944.CrossRefGoogle ScholarPubMed
212Sriwijitkamol, A, Coletta, DK, Wajcberg, E, Balbontin, GB, Reyna, SM, Barrientes, J, et al. Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 2007; 56: 836–48.CrossRefGoogle ScholarPubMed
213Ptitsyn, A, Hulver, M, Cefalu, W, York, D, Smith, SR. Unsupervised clustering of gene expression data points at hypoxia as possible trigger for metabolic syndrome. BMC Genomics 2006; 7: 318.CrossRefGoogle ScholarPubMed
214Lowes, BD, Baker, ML, Blaxall, BC. Gene expression profile of the recovering human heart. Eur Heart J 2007; 28: 522–24.CrossRefGoogle ScholarPubMed
215Krishnan, J, Suter, M, Windak, R, Krebs, T, Felley, A, Montessuit, C, et al. Activation of a HIF1alpha-PPARgamma axis underlies the integration of glycolytic and lipid anabolic pathways in pathologic cardiac hypertrophy. Cell Metab 2009; 9: 512–24.CrossRefGoogle ScholarPubMed
216Lionetti, V, Stanley, WC, Recchia, FA. Modulating fatty acid oxidation in heart failure. Cardiovasc Res 2011; 90: 202209.CrossRefGoogle ScholarPubMed
217Wang, Q, Donthi, RV, Wang, J, Lange, AJ, Watson, LJ, Jones, SP, et al. Cardiac phosphatase-deficient 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase increases glycolysis, hypertrophy, and myocyte resistance to hypoxia. Am J Physiol Heart Circ Physiol 2008; 294: H2889897.CrossRefGoogle ScholarPubMed
218Rajabi, M, Kassiotis, C, Razeghi, P, Taegtmeyer, H. Return to the fetal gene program protects the stressed heart: a strong hypothesis. Heart Fail Rev 2007 12: 331–43.CrossRefGoogle Scholar
219An, D, Rodrigues, B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 2006; 291: H1489506.CrossRefGoogle ScholarPubMed
220Kato, T, Niizuma, S, Inuzuka, Y, Kawashima, T, Okuda, J, Tamaki, Y, et al. Analysis of metabolic remodeling in compensated left ventricular hypertrophy and heart failure. Circ Heart Fail 2010; 3: 420–30.CrossRefGoogle ScholarPubMed
221Zhou, YT, Grayburn, P, Karim, A, Shimabukuro, M, Higa, M, Baetens, D, et al. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci USA. 2000; 97: 1784–789.CrossRefGoogle ScholarPubMed