1. Barker, DJ (1998)
In utero programming of chronic disease. Clin Sci (Lond) 95, 115–128.
2. Godfrey, KM & Barker, DJP (2001) Fetal programming and adult health. Public Health Nutr 4, 611–624.
3. O’Sullivan, L, Little, MH, Combes, AN, et al. (2012) Epigenetics and developmental programming of adult onset diseases. Pediatr Nephrol 27, 2175–2182.
4. Portha, B, Fournier, A, Ah Kioon, MD, et al. (2014) Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility. Biochimie 97, 1–15.
5. Huda, SS, Brodie, LE & Sattar, N (2010) Obesity in pregnancy: prevalence and metabolic consequences. Semin Fetal Neonatal Med 15, 70–76.
6. Jones, AP & Friedman, MI (1982) Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science 215, 1518–1519.
7. Siriwardhana, N, Kalupahana, NS, Cekanova, M, et al. (2013) Modulation of adipose tissue inflammation by bioactive food compounds. J Nutr Biochem 24, 613–623.
8. Lehr, S, Hartwig, S, Lamers, D, et al. (2012) Identification and validation of novel adipokines released from primary human. Mol Cell Proteomics 11, M111.010504.
9. Kim, SH & Plutzky, J (2016) Brown fat and browning for the treatment of obesity and related metabolic disorders. Diabetes Metab J 40, 12–21.
11. Fleming, NgM, Robinson, T, Thomson, M, et al. (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384, 766–781.
12. Claycombe, KJ, Vomhof-DeKrey, EE, Roemmich, JN, et al. (2015) Maternal low-protein diet causes body weight loss in male, neonate Sprague–Dawley rats involving UCP-1-mediated thermogenesis. J Nutr Biochem 26, 729–735.
13. Bruce, KD & Jonscher, KR (2018) Assessment of fatty liver in models of disease programming.
Methods Mol Biol
14. Szostak-Wegierek, D (2014) Intrauterine nutrition: long-term consequences for vascular health. Int J Womens Health 6, 647.
15. Rippe, C, Berger, K, Böiers, C, et al. (2000) Effect of high-fat diet, surrounding temperature, and enterostatin on uncoupling protein gene expression. Am J Physiol Endocrinol Metab 279, E293–E300.
16. Felipe, A, Villarroya, F & Mampel, T (1988) Effects of maternal hypocaloric diet feeding on neonatal rat brown adipose tissue. Neonatology 53, 105–112.
17. Chen, Y, Buyel, JJ & Hanssen, MJ (2016) Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity. Nat Commun 7, 11420.
18. Priego, T, Sánchez, J, García, AP, et al. (2013) Maternal dietary fat affects milk fatty acid profile and impacts on weight gain and thermogenic capacity of suckling rats. Lipids 48, 481–495.
19. Fromme, T & Klingenspor, M (2011) Uncoupling protein 1 expression and high-fat diets. Am J Physiol Regul Integr Comp Physiol 300, R1–R8.
20. van Marken Lichtenbelt, WD & Schrauwen, P (2011) Implications of nonshivering thermogenesis for energy balance regulation in humans. Am J Physiol Regul Integr Comp Physiol 301, R285–R296.
21. Rolfe, DF, Newman, JM, Buckingham, JA, et al. (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276, C692–C699.
22. Ouellet, V, Labbé, SM, Blondin, DP, et al. (2012) Brown adipose tissue oxidative metabolism contributles to energy expenditure during cold exposure in humans. J Clin Invest 122, 545.
23. Clarke, L, Bryant, MJ, Lomax, M, et al. (1997) Maternal manipulation of brown adipose tissue and liver development in the ovine fetus during late gestation. Br J Nutr 77, 871–883.
24. Vijgen, GHEJ, Bouvy, ND, Teule, GJJ, et al. (2011) Brown adipose tissue in morbidly obese subjects. PLoS ONE 6, 2–7.
25. Bartelt, A, Bruns, OT, Reimer, R, et al. (2011) Brown adipose tissue activity controls triglyceride clearance. Nat Med 17, 200–205.
26. Ricquier, D & Bouillaud, F (2000) The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 345, 161.
27. Symonds, ME, Dellschaft, N, Pope, M, et al. (2016) Theriogenology developmental programming, adiposity, and reproduction in ruminants. Theriogenology 86, 120–129.
28. Hayman, LL, Sciences, H & Boston, G (2011) A new connection between muscle and brown fat. J. Pediatr 158, 696–698.
29. Symonds, ME, Pope, M, Sharkey, D, et al. (2012) Adipose tissue and fetal programming. Diabetologia 55, 1597–1606.
30. Symonds, ME, Pope, M & Budge, H (2015) The ontogeny of brown adipose tissue. Annu Rev Nutr 35, 295–320.
31. Bartelt, A & Heeren, J (2014) Adipose tissue browning and metabolic health. Nat Rev Endocrinol 10, 24–36.
32. Seale, P, Bjork, B, Yang, W, et al. (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961–967.
33. Cypess, AM, Lehman, S, Williams, G, et al. (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360, 1509–1517.
34. Trayhurn, P & Jennings, G (1988) Nonshivering thermogenesis and the thermogenic capacity of brown fat in fasted and/or refed mice. Am J Physiol 254, R11–R16.
35. Kozak, LP (2010) Brown fat and the myth of diet-induced thermogenesis. Cell Metab 11, 263–267.
36. Kumar, MV, Sunvold, GD & Scarpace, PJ (1999) Dietary vitamin A supplementation in rats: suppression of leptin and induction of UCP1 mRNA. J Lipid Res 40, 824–829.
37. Jeyakumar, SM, Vajreswari, A & Giridharan, NV (2006) Chronic dietary vitamin A supplementation regulates obesity in an obese mutant WNIN/Ob rat model. Obesity 14, 52–59.
38. Ribot, J, Felipe, F, Bonet, ML, et al. (2004) Retinoic acid administration and vitamin A status modulate retinoid X receptor alpha and retinoic acid receptor alpha levels in mouse brown adipose tissue. Mol Cell Biochem 266, 25–30.
39. Kumar, MV & Scarpace, PJ (1998) Differential effects of retinoic acid on uncoupling protein-1 and leptin gene expression. J Endocrinol 157, 237–243.
40. Scarpace, PJ, Matheny, M, Moore, RL, et al. (2000) Modulation of uncoupling protein 2 and uncoupling protein 3: regulation by denervation, leptin and retinoic acid treatment. J Endocrinol 164, 331–337.
41. Felipe, F, Bonet, ML, Ribot, J, et al. (2003) Up-regulation of muscle uncoupling protein 3 gene expression in mice following high fat diet, dietary vitamin A supplementation and acute retinoic acid-treatment. Int J Obes Relat Metab Disord 27, 60–69.
42. Jobgen, W, Meininger, CJ, Jobgen, SC, et al. (2009) Dietary L-arginine supplementation reduces white fat gain and enhances skeletal muscle and brown fat masses in diet-induced obese rats. J Nutr 139, 230–237.
43. Konishi, Y, Koosaka, Y, Maruyama, R, et al. (2015) ʟ-Ornithine intake affects sympathetic nerve outflows and reduces body weight and food intake in rats. Brain Res Bull 111, 48–52.
44. Kanamoto, Y, Yamashita, Y, Nanba, F, et al. (2011) A black soybean seed coat extract prevents obesity and glucose intolerance by up-regulating uncoupling proteins and down-regulating inflammatory cytokines in high-fat diet-fed mice. J Agric Food Chem 59, 8985–8993.
45. Andrade, JMO, Frade, ACM, Guimarães, JB, et al. (2014) Resveratrol increases brown adipose tissue thermogenesis markers by increasing SIRT1 and energy expenditure and decreasing fat accumulation in adipose tissue of mice fed a standard diet. Eur J Nutr 53, 1503–1510.
46. Alberdi, G, Rodríguez, VM, Miranda, J, et al. (2013) Thermogenesis is involved in the body-fat lowering effects of resveratrol in rats. Food Chem 141, 1530–1535.
47. Ku, CR, Cho, YH, Hong, Z, et al. (2016) The Effects of High Fat Diet and Resveratrol on Mitochondrial Activity of Brown Adipocytes. Endocrinol Metab (Seoul) 31, 328–335.
48. Crespillo, A, Alonso, M, Vida, M, et al. (2011) Reduction of body weight, liver steatosis and expression of stearoyl-CoA desaturase 1 by the isoflavone daidzein in diet-induced obesity. Br J Pharmacol 164, 1899–1915.
49. Kamiya, T, Nagamine, R, Sameshima-Kamiya, M, et al. (2012) The isoflavone-rich fraction of the crude extract of the Puerariae flower increases oxygen consumption and BAT UCP1 expression in high-fat diet-fed mice. Glob J Health Sci 4, 147–155.
50. Nirengi, S, Amagasa, S, Homma, T, et al. (2016) Daily ingestion of catechin-rich beverage increases brown adipose tissue density and decreases extramyocellular lipids in healthy young women. Springerplus 5, 1363.
51. Nomura, S, Ichinose, T, Jinde, M, et al. (2008) Tea catechins enhance the mRNA expression of uncoupling protein 1 in rat brown adipose tissue. J Nutr Biochem 19, 840–847.
52. Kudo, N, Arai, Y, Suhara, Y, et al. (2015) A single oral administration of theaflavins increases energy expenditure and the expression of metabolic genes. PLOS ONE 10, 1–9.
53. Matsumura, Y, Nakagawa, Y, Mikome, K, et al. (2014) Enhancement of energy expenditure following a single oral dose of flavan-3-ols associated with an increase in catecholamine secretion. PLOS ONE 9, e112180.
54. Smith, SB, Carstens, GE, Randel, RD, et al. (1998) Brown adipose tissue development and metabolism in ruminants. J Anim Sci 82, 942–954.
55. Sellayah, D, Bharaj, P & Sikder, D (2011) Orexin is required for brown adipose tissue development, differentiation, and function. Cell Metab 14, 478–490.
56. Feldmann, HM, Golozoubova, V & Cannon, B (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9, 203–209.
57. Cannon, B & Nedergaard, J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84, 277–359.
58. Ho, DJ, Calingasan, NY & Wille, E (2010) Resveratrol protects against peripheral deficits in a mouse model of Huntington’s disease. Exp Neurol 225, 74–84.
59. Liang, X, Yang, Q, Zhang, L, et al. (2016) Maternal high-fat diet during lactation impairs thermogenic function of brown adipose tissue in offspring mice. Sci Rep 6, 34345.
60. Oi-Kano, Y, Kawada, T, Watanabe, T, et al. (2016) Extra virgin olive oil increases uncoupling protein 1 content in brown adipose tissue and enhances noradrenaline and adrenaline secretions in rats. J Nutr Biochem 18, 685–692.
61. Rodriguez, VM, Portillo, MP, Pico, C, et al. (2002) Olive oil feeding up-regulates uncoupling protein genes in rat brown adipose tissue and skeletal muscle. Am J Clin Nutr 75, 213–220.
62. Vögler, O, Ló Pez-Bellan, A, Alemany, R, et al. (2008) Structure–effect relation of C18 long-chain fatty acids in the reduction of body weight in rats. Int J Obes (Lond) 32, 464–473.
63. Clarke, SD (2000) Polyunsaturated fatty acid regulation of gene transcription: a mechanism to improve energy balance and insulin resistance. Br J Nutr 83, Suppl. 1, S59–S66.
64. Kunešová, M, Hlavatý, P, Tvrzická, E, et al. (2012) Fatty acid composition of adipose tissue triglycerides after weight loss and weight maintenance: the DIOGENES study. Physiol Res 61, 597–607.
65. Mori, TA, Bao, DQ, Burke, V, et al. (1999) Dietary fish as a major component of a weight-loss diet: Effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects. Am J Clin Nutr 70, 817–825.
66. Bargut, TCL, Silva-e-Silva, ACAG, Souza-Mello, V, et al. (2016) Mice fed fish oil diet and upregulation of brown adipose tissue thermogenic markers. Eur J Nutr 55, 159–169.
67. Bargut, TCL, Frantz, EDC, Mandarim-De-Lacerda, CA, et al. (2014) Effects of a diet rich in n-3 polyunsaturated fatty acids on hepatic lipogenesis and beta-oxidation in mice. Lipids 49, 431–444.
68. Suchankova, G, Tekle, M, Saha, AK, et al. (2005) Dietary polyunsaturated fatty acids enhance hepatic AMP-activated protein kinase activity in rats. Biochem Biophys Res Commun 28, 851–858.
69. Rodríguez-Cruz, M & Serna, DS (2017) Nutrigenomics of ω-3 fatty acids: regulators of the master transcription factors. Nutrition 41, 90–96.
70. Hondares, E, Rosell, M, Díaz-Delfín, J, et al. (2011) Peroxisome proliferator-activated receptor α (PPARα) induces PPARγ coactivator 1α (PGC-1α) gene expression and contributes to thermogenic activation of brown fat: involvement of PRDM16. J Biol Chem 286, 43112–43122.
71. Festuccia, WT, Blanchard, P, Richard, D, et al. (2010) Basal adrenergic tone is required for maximal stimulation of rat brown adipose tissue UCP1 expression by chronic PPAR-gamma activation. Am J Physiol Regul Integr Comp Physiol 299, R159–R167.
72. Cao, W, Daniel, KW, Robidoux, J, et al. (2004) p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol Cell Biol 24, 3057–3067.
73. Zhao, M & Chen, X (2014) Eicosapentaenoic acid promotes thermogenic and fatty acid storage capacity in mouse subcutaneous adipocytes. Biochem Biophys Res Commun 450, 1446–1451.
74. Lee, P, Werner, C, Kebebew, E, et al. (2013) Functional thermogenic beige adipogenesis is inducible in human neck fat. Int J Obes (Lond) 38, 170–176.
75. Pahlavani, M, Razafimanjato, F, Ramalingam, L, et al. (2017) Eicosapentaenoic acid regulates brown adipose tissue metabolism in high-fat-fed mice and in clonal brown adipocytes. J Nutr Biochem 39, 101–109.
76. Waldén, TB, Hansen, IR, Timmons, JA, Cannon, B & Nedergaard, J (2011) Recruited vs. nonrecruited molecular signatures of brown,‘brite,’ and white adipose tissues. Am J Physiol Endocrinol and Metab 302, E19–E31.
77. Qin, Y, Zhou, Y, Chen, SH, et al. (2015) Fish oil supplements lower serum lipids and glucose in correlation with a reduction in plasma fibroblast growth factor 21 and prostaglandin E2 in nonalcoholic fatty liver disease associated with hyperlipidemia: a randomized clinical trial. PLOS ONE 10, e0133496.
78. Quesada-López, T, Cereijo, R, Turatsinze, JV, et al. (2016) The lipid sensor GPR120 promotes brown fat activation and FGF21 release from adipocytes. Nat Commun 7, 13479.
79. Shore, A, Karamitri, A, Kemp, P, et al. (2010) Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia 53, 1164–1173.
80. Seki, Y, Williams, L, Vuguin, PM, et al. (2012) Minireview: Epigenetic programming of diabetes and obesity: animal models. Endocrinology 153, 1031–1038.
81. Shi, T, Wang, F, Stieren, E, et al. (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280, 13560–13567.
82. Boutant, M, Joffraud, M, Kulkarni, SS, et al. (2015) SIRT1 enhances glucose tolerance by potentiating brown adipose tissue function. Mol Metab 4, 118–131.
83. Zha, L, Li, F, Wu, R, et al. (2015) The histone demethylase UTX promotes brown adipocyte thermogenic program via coordinated regulation of H3K27 demethylation and acetylation. J Biol Biochem 290, 25151–25163.
84. Pfeifer, A & Lehmann, H (2010) Pharmacology & therapeutics pharmacological potential of RNAi — focus on miRNA. Pharmacol Ther 126, 217–227.
85. Trajkovski, M & Lodish, H (2013) MicroRNA networks regulate development of brown adipocytes. Trends Endocrinol Metab 24, 442–450.
86. Laiglesia, LM, Lorente-Cebrián, S, Prieto-Hontoria, PLM, et al. (2016) Eicosapentaenoic acid promotes mitochondrial biogenesis and beige-like features in subcutaneous adipocytes from overweight subjects. J Nutr Biochem 37, 76–82.
87. Kim, J, Okla, M, Erickson, A, et al. (2016) Eicosapentaenoic acid potentiates brown thermogenesis through FFAR4-dependent up-regulation of miR-30b and miR-378. J Biol Chem 291, 20551–20562.
88. Godfrey, KM (1998) Maternal regulation of fetal development and health in adult life. Eur J Obstet Gynecol Reprod Biol 78, 141–150.
89. Gabory, A, Vigé, A, Ferry, L, et al. (2014) Hormones, intrauterine health and programming. Res Perspect Endocr Interact 12, 71–91.
90. Innis, SM (2011) Metabolic programming of long-term outcomes due to fatty acid nutrition in early life. Matern Child Nutr 7, Suppl. 2, 112–123.
91. Novak, EM, Keller, BO & Innis, SM (2012) Metabolic development in the liver and the implications of the n-3 fatty acid supply. Am J Physiol Gastrointest Liver Physiol 302, G250–G259.
92. Larqué, E, Ruiz-Palacios, M & Koletzko, B (2013) Placental regulation of fetal nutrient supply. Curr Opin Clin Nutr Metab Care 16, 292–297.
93. Fonseca, BM, Correia-da-silva, G & Teixeira, NA (2012) The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period. Reprod Biol 12, 97–118.
94. Mennitti, LV, Oliveira, JL, Morais, CA, et al. (2015) Type of fatty acids in maternal diets during pregnancy and/or lactation and metabolic consequences of the offspring. J Nutr Biochem 26, 99–111.
95. del Bas, JM, Crescenti, A, Arola-Arnal, A, et al. (2015) Grape seed procyanidin supplementation to rats fed a high-fat diet during pregnancy and lactation increases the body fat content and modulates the inflammatory response and the adipose tissue metabolism of the male offspring in youth. Int J Obes (Lond) 39, 7–15.
96. Todaka, E, Sakurai, K, Fukata, H, et al. (2005) Fetal exposure to phytoestrogens – the difference in phytoestrogen status between mother and fetus. Environ Res 99, 195–203.
97. Morais, CA, Oyama, LM, de Moura Conrado, R, et al. (2015) Polyphenols-rich fruit in maternal diet modulates inflammatory markers and the gut microbiota and improves colonic expression of ZO-1 in offspring. Food Res Int 77, 186–193.
98. Mukai, Y, Sun, Y & Sato, S (2013) Azuki bean polyphenols intake during lactation upregulate AMPK in male rat offspring exposed to fetal malnutrition. Nutrition 29, 291–297.
99. van Hoffen, E, Ruiter, B, Faber, J, et al. (2009) A specific mixture of short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy 64, 484–487.
100. Gohir, W, Ratcliffe, EM, Sloboda, DM, et al. (2014) Of the bugs that shape us: maternal obesity, the gut microbiome, and long-term disease risk. Pediatr Res 77, 196–204.
101. Symonds, ME (2013) Brown adipose tissue growth and development. Scientifica (Cairo) 2013, 305763.
102. Sellayah, D & Sikder, D (2014) Orexin restores aging-related brown adipose tissue dysfunction in male mice. Endocrinology 155, 485–501.
103. Giralt, M & Villarroya, F (2013) White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154, 2992–3000.
104. Budge, H (2004) Nutritional manipulation of fetal adipose tissue deposition and uncoupling protein 1 messenger rna abundance in the sheep: differential effects of timing and duration. Biol Reprod 71, 359–365.
105. Ojha, S, Robinson, L, Yazdani, M, et al. (2013) Brown adipose tissue genes in pericardial adipose tissue of newborn sheep are downregulated by maternal nutrient restriction in late gestation. Pediatr Res 74, 246–251.
106. Ojha, S, Symonds, ME & Budge, H (2015) Suboptimal maternal nutrition during early-to-mid gestation in the sheep enhances pericardial adiposity in the near-term fetus. Reprod Fertil Dev 27, 1205–1212.
107. Sellayah, D, Dib, L, Anthony, FW, et al. (2014) Effect of maternal protein restriction during pregnancy and postweaning high-fat feeding on diet-induced thermogenesis in adult mouse offspring. Eur J Nutr 53, 1523–1531.
108. Argentato, PP, Morais, CA, Santamarina, AB, et al. (2017) Jussara (Euterpe edulis Mart.) supplementation during pregnancy and lactation modulates UCP-1 and inflammation biomarkers induced by trans-fatty acids in the brown adipose tissue of offspring. Clin Nutr Exp 12, 50–65.
109. Bayol, SA, Simbi, BH, Bertrand, JA, et al. (2008) Offspring from mothers fed a ‘junk food’ diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol 586, 3219–3230.
110. 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. J. Physiol 567, 951–961.
111. Sun, B, Purcell, RH, Terrillion, CE, et al. (2012) Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 61, 2833–2841.
112. Turdi, S, Ge, W, Hu, N, et al. (2012) Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects. J Mol Cell Cardiol 55, 117–129.