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Developmental origins of obesity: a sympathoadrenal perspective

International Journal of Obesity volume 30, pages S41–S49 (2006)Cite this article

Abstract

Environmental exposures at crucial points in development permanently alter sympathoadrenal function in mammals. Both the sympathetic innervation of peripheral tissues and the responsiveness of sympathetic nerves and adrenal medulla to standard stimuli are susceptible to modification by exposures in early life. Several conditions studied in the laboratory, including environmental temperature, litter size and maternal nutrition, in addition to affecting sympathoadrenal function also produce larger, fatter offspring, raising the possibility that developmental programming of the sympathetic nervous system (SNS) may contribute to acquisition of an obese phenotype. The specific changes noted in all three circumstances include evidence of an increase in sympathetic innervation in pancreas and retroperitoneal fat. By contrast, SNS development is impaired in experimental models of intrauterine growth retardation. Although the physiological implications of increased sympathetic innervation in pancreas and retroperitoneal fat are not fully understood, these changes seen in animals reared at cool temperatures, in small litters or by mothers fed refined carbohydrate diets likely reflect an early enhancement of the offspring's capacity to take up and store glucose. If so, the tendency of these animals to gain weight and accumulate fat may represent an adaptive response to ‘over-nutrition’ in early life.

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References

  1. Hubel DH, Wiesel TN . The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol (London) 1970; 206: 419–436.

    Article  CAS  Google Scholar 

  2. Thoenen H . Neurotrophins and neuronal plasticity. Science 1995; 270: 593–598.

    Article  CAS  PubMed  Google Scholar 

  3. Moore DR . Postnatal development of the mammalian central auditory system and the neural consequences of auditory deprivation. Acta Otolaryngol Suppl 1985; 421: 19–30.

    Article  CAS  PubMed  Google Scholar 

  4. Kempermann G, van Praag H, Gage FH . Activity-dependent regulation of neuronal plasticity and self repair. Prog Brain Res 2000; 127: 35–48.

    Article  CAS  PubMed  Google Scholar 

  5. Hendry IA, Campbell J . Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment. J Neurocytol 1976; 5: 351–360.

    Article  CAS  PubMed  Google Scholar 

  6. Oppenheim RW . Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14: 453–501.

    Article  CAS  PubMed  Google Scholar 

  7. Seckl JR, Meaney MJ . Glucocorticoid programming. Ann NY Acad Sci 2004; 1032: 63–84.

    Article  CAS  PubMed  Google Scholar 

  8. Kuno Y . Human perspiration. Charles C Thomas: Springfield, IL, 1956.

    Google Scholar 

  9. Young JB, Weiss J, Boufath N . Effects of rearing temperature on sympathoadrenal activity in young adult rats. Am J Physiol 2002; 283: R1198–R1209.

    Google Scholar 

  10. Young JB . Developmental plasticity in SNS response to fasting in adipose tissues of male rats. Metabolism 2003; 52: 1621–1626.

    Article  CAS  PubMed  Google Scholar 

  11. Young JB . Effects of neonatal handling on sympathoadrenal activity and body composition in adult male rats. Am J Physiol 2000; 279: R1745–R1752.

    CAS  Google Scholar 

  12. Hashimoto M, Watanabe T, Fujioka T, Tan N, Yamashita H, Nakamura S . Modulating effects of prenatal stress on hyperthermia induced in adult rat offspring by restraint or LPS-induced stress. Physiol Behav 2001; 73: 125–132.

    Article  CAS  PubMed  Google Scholar 

  13. Nyirenda MJ, Welberg LAM, Seckl JR . Programming hyperglycaemia in the rat through prenatal exposure to glucocorticoids-fetal effect or maternal influence? J Endocrinol 2001; 170: 653–660.

    Article  CAS  PubMed  Google Scholar 

  14. Raff H, Lee JJ, Widmaier EP, Oaks MK, Engeland WC . Basal and adrenocorticotropin-stimulated corticosterone in the neonatal rat exposed to hypoxia from birth: modulation by chemical sympathectomy. Endocrinology 2004; 145: 79–86.

    Article  CAS  PubMed  Google Scholar 

  15. Peyronnet J, Dalmaz Y, Ehrström M, Mamet J, Roux J-C, Pequignot J-M et al. Long-lasting adverse effects of prenatal hypoxia on developing autonomic nervous system and cardiovascular parameters in rats. Pflügers Arch 2002; 443: 858–865.

    Article  CAS  PubMed  Google Scholar 

  16. Mamet J, Peyronnet J, Roux J-C, Perrin D, Cottet-Emard J-M, Pequignot J-M et al. Long-term prenatal hypoxia alters maturation of adrenal medulla in rat. Pediatr Res 2002; 51: 207–214.

    Article  PubMed  Google Scholar 

  17. Bian X, Seidler FJ, Slotkin TA . Fetal dexamethasone exposure interferes with establishment of cardiac noradrenergic innervation and sympathetic activity. Teratology 1993; 47: 109–117.

    Article  CAS  PubMed  Google Scholar 

  18. Segar JL, Lumbers ER, Nuyt AM, Smith OJ, Robillard JE . Effect of antenatal glucocorticoids on sympathetic nerve activity at birth in preterm sheep. Am J Physiol 1998; 274: R160–R167.

    CAS  PubMed  Google Scholar 

  19. Oyama K, Padbury J, Martinez A, Chappell B, Stein H, Humme J . Effects of fetal growth retardation on the development of central and peripheral catecholaminergic pathways in the sheep. J Dev Physiol 1992; 18: 217–222.

    CAS  PubMed  Google Scholar 

  20. Sanders M, Fazzi G, Janssen G, Blanco C, De Mey J . Prenatal stress changes rat arterial adrenergic reactivity in a regionally selective manner. Eur J Pharmacol 2004; 488: 147–155.

    Article  CAS  PubMed  Google Scholar 

  21. Jansson T, Lambert GW . Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous system activity in the rat at 3–4 months of age. J Hypertens 1999; 17: 1239–1248.

    Article  CAS  PubMed  Google Scholar 

  22. Alexander BT, Hendon AE, Ferril G, Dwyer TM . Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 2005; 45: 754–758.

    Article  CAS  PubMed  Google Scholar 

  23. Gottesfeld Z, Christie R, Felten DL, LeGrue SJ . Prenatal ethanol exposure alters immune capacity and noradrenergic synaptic transmission in lymphoid organs of the adult mouse. Neuroscience 1990; 35: 185–194.

    Article  CAS  PubMed  Google Scholar 

  24. Zimmerberg B, Carson EA, Kaplan LJ, Zuniga JA, True RC . Role of noradrenergic innervation of brown adipose tissue in thermoregulatory deficits following prenatal alcohol exposure. Alcohol Clin Exp Res 1993; 17: 418–422.

    Article  CAS  PubMed  Google Scholar 

  25. Navarro HA, Seidler FJ, Whitmore WL, Slotkin TA . Prenatal exposure to nicotine via maternal infusion: effects on development of catecholamine systems. J Pharmacol Exp Ther 1988; 244: 940–944.

    CAS  PubMed  Google Scholar 

  26. Slotkin TA, Cho H, Whitmore WL . Effects of prenatal nicotine exposure on neuronal development: selective actions on central and peripheral catecholaminergic pathways. Brain Res Bull 1987; 18: 601–611.

    Article  CAS  PubMed  Google Scholar 

  27. Wong T, Wickström R, Holgert H . Chronic prenatal nicotine exposure alters enkephalin mRNA regulation in the perinatal rat adrenal medulla. Pediatr Res 2003; 53: 814–816.

    Article  CAS  PubMed  Google Scholar 

  28. Dailey JW . Effects of maternal chlorpromazine on offspring nervous system development. Neuropharmacology 1978; 17: 583–587.

    Article  CAS  PubMed  Google Scholar 

  29. Shinohara Y, Matsumoto A, Mori T . Effects of prenatal exposure to diethylstilbestrol on the sympathetic nervous system in the rat ovary. Neurosci Lett 1998; 255: 123–126.

    Article  CAS  PubMed  Google Scholar 

  30. Conboy VB, Santer RM, Swift GL . Effects of prenatal undernutrition on prevertebral sympathetic neurons in the rat: a morphological and fluorescence histochemical study. J Anat 1987; 154: 47–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Santer RM, Conboy VB . Prenatal undernutrition permanently decreases enteric neuron number and sympathetic innervation of Auerbach's plexus in the rat. J Anat 1990; 168: 57–62.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Petry CJ, Dorling MW, Wang CL, Pawlak DB, Ozanne SE . Catecholamine levels and receptor expression in low protein rat offspring. Diabetes Med 2000; 17: 848–853.

    Article  CAS  Google Scholar 

  33. Semafuko WEB, Rutledge CO, Dixon WR . Effect of dietary lipids on myocardial norepinephrine content and field stimulation-mediated release of norepinephrine from perfused neonatal and adult rat hearts. J Cardiovasc Pharmacol 1987; 10: 16–23.

    Article  CAS  PubMed  Google Scholar 

  34. Seidler FJ, Bell JM, Slotkin TA . Undernutrition and overnutrition in the neonatal rat: long-term effects on noradrenergic pathways in brain regions. Pediatr Res 1990; 27: 191–197.

    Article  CAS  PubMed  Google Scholar 

  35. Young JB . Effects of litter size on sympathetic activity in young adult rats. Am J Physiol 2002; 282: R1113–R1121.

    Article  CAS  Google Scholar 

  36. Jänig W, McLachlan EM . Characteristics of function-specific pathways in the sympathetic nervous system. Trends Neurosci 1992; 15: 475–481.

    Article  PubMed  Google Scholar 

  37. Snitker S, Macdonald I, Ravussin E, Astrup A . The sympathetic nervous system and obesity: role in aetiology and treatment. Obes Rev 2000; 1: 5–15.

    Article  CAS  PubMed  Google Scholar 

  38. Esler M, Rumantir M, Wiesner G, Kaye D, Hastings J, Lambert G . Sympathetic nervous system and insulin resistance: from obesity to diabetes. Am J Hypertens 2001; 14: 304S–309S.

    Article  CAS  PubMed  Google Scholar 

  39. van Baak MA . The peripheral sympathetic nervous system in human obesity. Obes Rev 2001; 2: 3–14.

    Article  CAS  PubMed  Google Scholar 

  40. Rahmouni K, Correia MLG, Haynes WG, Mark AL . Obesity-associated hypertension: new insights into mechanisms. Hypertension 2005; 45: 9–14.

    Article  CAS  PubMed  Google Scholar 

  41. Ingram DL . Adaptations to ambient temperature in growing pigs. Pflügers Arch 1977; 367: 257–264.

    Article  CAS  PubMed  Google Scholar 

  42. Heath M, Ingram DL . Thermoregulatory heat production in cold-reared and warm-reared pigs. Am J Physiol 1983; 244: R273–R278.

    CAS  PubMed  Google Scholar 

  43. Hahn P . Effect of environmental temperatures on the development of thermoregulatory mechanisms in infant rats. Nature 1956; 178: 96–97.

    Article  CAS  PubMed  Google Scholar 

  44. Cooper KE, Ferguson AV, Veale WL . Modification of thermoregulatory responses in rabbits reared at elevated environmental temperatures. J Physiol (London) 1980; 303: 165–172.

    Article  CAS  Google Scholar 

  45. Jensen RA, Davis JL, Shnerson A . Early experience facilitates the development of temperature regulation in the cat. Dev Psychobiol 1980; 13: 1–6.

    Article  CAS  PubMed  Google Scholar 

  46. Bertin R, Mouroux I, De Marco F, Portet R . Norepinephrine turnover in brown adipose tissue of young rats: effects of rearing temperature. Am J Physiol 1990; 259: R90–R96.

    CAS  PubMed  Google Scholar 

  47. Morrison SF, Ramamurthy S, Young JB . Reduced rearing temperature augments responses in sympathetic outflow to brown adipose tissue. J Neurosci 2000; 20: 9264–9271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Young JB, Shimano Y . Effects of rearing temperature on body weight and abdominal fat in male and female rats. Am J Physiol 1998; 274: R398–R405.

    CAS  PubMed  Google Scholar 

  49. Young JB, Weiss J, Boufath N . Effects of dietary monosaccharides on SNS activity in adipose tissues of male rats. Diabetes 2004; 53: 1271–1278.

    Article  CAS  PubMed  Google Scholar 

  50. Valet P, Grujic D, Wade J, Ito M, Zingaretti MC, Soloveva V et al. Expression of human α2-adrenergic receptors in adipose tissue of β3-adrenergic receptor-deficient mice promotes diet-induced obesity. J Biol Chem 2000; 275: 34797–34802.

    Article  CAS  PubMed  Google Scholar 

  51. Lemonnier D, Suquet J-P, Aubert R, Rosselin G . Long term effect of mouse neonate food intake on adult body composition, insulin and glucose serum levels. Horm Metab Res 1973; 5: 223–224.

    Article  CAS  PubMed  Google Scholar 

  52. Oscai LB . Dietary-induced severe obesity: a rat model. Am J Physiol 1982; 242: R212–R215.

    CAS  PubMed  Google Scholar 

  53. Yagil R, Etzion Z, Berlyne GM . Changes in rat milk quantity and quality due to variations in litter size and high ambient temperature. Lab Anim Sci 1976; 26: 33–37.

    CAS  PubMed  Google Scholar 

  54. Russell JA . Milk yield, suckling behaviour and milk ejection in the lactating rat nursing litters of different sizes. J Physiol (London) 1980; 303: 403–415.

    Article  CAS  Google Scholar 

  55. Young JB, Landsberg L . Stimulation of the sympathetic nervous system during sucrose feeding. Nature 1977; 269: 615–617.

    Article  CAS  PubMed  Google Scholar 

  56. Young JB, Landsberg L . Effect of diet and cold exposure on norepinephrine turnover in pancreas and liver. Am J Physiol 1979; 236: E524–E533.

    CAS  PubMed  Google Scholar 

  57. Vander Tuig JG, Romsos DR . Effects of dietary carbohydrate, fat and protein on norepinephrine turnover in rats. Metabolism 1984; 33: 26–33.

    Article  CAS  PubMed  Google Scholar 

  58. Walgren MC, Young JB, Kaufman LN, Landsberg L . The effects of various carbohydrates on sympathetic activity in heart and interscapular brown adipose tissue (IBAT) of the rat. Metabolism 1987; 36: 585–594.

    Article  CAS  PubMed  Google Scholar 

  59. Dulloo AG, Young JB, Landsberg L . Sympathetic nervous system responses to cold exposure and diet in rat skeletal muscle. Am J Physiol 1988; 255: E180–E188.

    CAS  PubMed  Google Scholar 

  60. Young JB, Landsberg L . Impaired suppression of sympathetic activity during fasting in the gold thioglucose-treated mouse. J Clin Invest 1980; 65: 1086–1094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Dulloo AG, Young JB . Effects of monosodium glutamate and gold thioglucose on dietary regulation of sympathetic nervous system activity in rodents. Metabolism 1991; 40: 113–121.

    Article  CAS  PubMed  Google Scholar 

  62. Plagemann A, Heidrich I, Götz F, Rohde W, Dörner G . Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding. Exp Clin Endocrinol 1992; 99: 154–158.

    Article  CAS  PubMed  Google Scholar 

  63. Plagemann A, Harder T, Rake A, Janert U, Melchior K, Rohde W et al. Morphological alterations of hypothalamic nuclei due to intrahypothalamic hyperinsulinism in newborn rats. Int J Dev Neurosci 1999; 17: 37–44.

    Article  CAS  PubMed  Google Scholar 

  64. Jovanovic-Peterson L, Fuhrmann K, Hedden K, Walker L, Peterson CM . Maternal milk and plasma glucose and insulin levels: studies in normal and diabetic subjects. J Am Coll Nutr 1989; 8: 125–131.

    Article  CAS  PubMed  Google Scholar 

  65. Mosinger B, Placer Z, Koldovsky O . Passage of insulin through the wall of the gastro-intestinal tract of the infant rat. Nature 1959; 184: 1245–1246.

    Article  CAS  PubMed  Google Scholar 

  66. Young JB, Morrison SF . Effects of fetal and neonatal environment on sympathetic nervous system development. Diabetes Care 1998; 21 (Suppl 2): B156–B160.

    PubMed  Google Scholar 

  67. Winick M, Noble A . Cellular response in rats during malnutrition at various ages. J Nutr 1966; 89: 300–306.

    Article  CAS  PubMed  Google Scholar 

  68. Zamenhof S, Van Marthens E, Margolis FL . DNA (cell number) and protein in neonatal brain: alteration by maternal dietary protein restriction. Science 1968; 160: 322–323.

    Article  CAS  PubMed  Google Scholar 

  69. Newman RW, Munro EH . The relation of climate and body size in US males. Am J Phys Anthropol 1955; 13: 1–17.

    Article  CAS  PubMed  Google Scholar 

  70. Phillips DIW, Young JB . Birth weight, climate at birth and the risk of obesity in adult life. Int J Obes 2000; 24: 281–287.

    Article  CAS  Google Scholar 

  71. Lawlor DA, Davey Smith G, Mitchell R, Ebrahim S . Temperature at birth, coronary heart disease, and insulin resistance: cross sectional analyses of the British women's heart and health study. Heart 2004; 90: 381–388.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Watkins B, Willoughby K, Waller G, Serpell L, Lask B . Pattern of birth in anorexia nervosa. I: Early-onset cases in the United Kingdom. Int J Eat Disord 2002; 32: 11–17.

    Article  PubMed  Google Scholar 

  73. Willoughby K, Watkins B, Beumont P, Maguire S, Lask B, Waller G . Pattern of birth in anorexia nervosa. II: A comparison of early-onset cases in the southern and northern hemispheres. Int J Eat Disord 2002; 32: 18–23.

    Article  PubMed  Google Scholar 

  74. Waller G, Meyer C, van Hanswijck de Jonge L . Early environmental influences on restrictive eating pathology among nonclinical females: the role of temperature at birth. Int J Eat Disord 2001; 30: 204–208.

    Article  CAS  PubMed  Google Scholar 

  75. van Hanswijck de Jonge L, Meyer C, Smith K, Waller G . Environmental temperature during pregnancy and eating attitudes during teenage years: a replication and extension study. Int J Eat Disord 2001; 30: 413–420.

    Article  CAS  PubMed  Google Scholar 

  76. van Hanswijck de Jonge L, Waller G . Influence of environmental temperatures during gestation and at birth on eating characteristics in adolescence: a replication and extension study. Appetite 2002; 38: 181–187.

    Article  CAS  PubMed  Google Scholar 

  77. Kärki NT . The urinary excretion of noradrenaline and adrenaline in different age groups, its diurnal variation and the effect of muscular work on it. Acta Physiol Scand Suppl 1956; 132: 1–96.

    Google Scholar 

  78. Johansson G . Sex differences in the catecholamine output of children. Acta Physiol Scand 1972; 85: 569–572.

    Article  CAS  PubMed  Google Scholar 

  79. Frankenhaeuser M, Dunne E, Lundberg U . Sex differences in sympathetic-adrenal medullary reactions induced by different stressors. Psychopharmacology 1976; 47: 1–5.

    Article  CAS  PubMed  Google Scholar 

  80. Davidson L, Vandongen R, Rouse IL, Beilin LJ, Tunney A . Sex-related differences in resting and stimulated plasma noradrenaline and adrenaline. Clin Sci 1984; 67: 347–352.

    Article  CAS  Google Scholar 

  81. Lakatua DJ, Nicolau GY, Bogdan C, Plinga L, Jachimowicz A, Sackett-Lundeen L et al. Chronobiology of catecholamine excretion in different age groups. Prog Clin Biol Res 1987; 227B: 31–50.

    CAS  PubMed  Google Scholar 

  82. Williams PD, Puddey IB, Beilin LJ, Vandongen R . Genetic influences on plasma catecholamines in human twins. J Clin Endocrinol Metab 1993; 77: 794–799.

    CAS  PubMed  Google Scholar 

  83. Amiel SA, Maran A, Powrie JK, Umpleby AM, Macdonald IA . Gender differences in counterregulation to hypoglycemia. Diabetologia 1993; 36: 460–464.

    Article  CAS  PubMed  Google Scholar 

  84. Gallen IW, Rosa RM, Esparaz DY, Young JB, Robertson GL, Batlle D et al. On the mechanism of the effects of potassium restriction on blood pressure and renal sodium excretion. Am J Kidney Dis 1998; 31: 19–27.

    Article  CAS  PubMed  Google Scholar 

  85. Del Rio G, Carani C, Bonati M, Marrama P, Della Casa L . Sexual dimorphism of the autonomic nervous system response to weight loss in obese patients. Int J Obes 1992; 16: 897–903.

    CAS  Google Scholar 

  86. Herrera E, Knopp RH, Freinkel N . Urinary excretion of epinephrine and norepinephrine during fasting in late pregnancy in the rat. Endocrinology 1969; 84: 447–450.

    Article  CAS  PubMed  Google Scholar 

  87. Landsberg L, Young JB . Fasting, feeding and regulation of the sympathetic nervous system. N Engl J Med 1978; 298: 1295–1301.

    Article  CAS  PubMed  Google Scholar 

  88. D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller J-F . Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol Reprod Dev 2001; 59: 265–276.

    Article  CAS  PubMed  Google Scholar 

  89. Pieau C, Dorizzi M . Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J Endocrinol 2004; 181: 367–377.

    Article  CAS  PubMed  Google Scholar 

  90. Jeyasuria P, Place AR . Embryonic brain-gonadal axis in temperature-dependent sex determination of reptiles: a role for P450 aromatase (CYP19). J Exp Zool 1998; 281: 428–449.

    Article  CAS  PubMed  Google Scholar 

  91. Baroiller JF, D'Cotta H . Environment and sex determination in farmed fish. Comp Biochem Physiol (C) 2001; 130: 399–409.

    CAS  Google Scholar 

  92. Jones AP, Dayries M . Maternal hormone manipulations and the development of obesity in rats. Physiol Behav 1990; 47: 1107–1110.

    Article  CAS  PubMed  Google Scholar 

  93. Plagemann A, Heidrich I, Götz F, Rohde W, Dörner G . Lifelong enhanced diabetes susceptibility and obesity after temporary intrahypothalamic hyperinsulinism during brain organization. Exp Clin Endocrinol 1992; 99: 91–95.

    Article  CAS  PubMed  Google Scholar 

  94. Harder T, Plagemann A, Rohde W, Dörner G . Syndrome X-like alterations in adult female rats due to neonatal insulin treatment. Metabolism 1998; 47: 855–862.

    Article  CAS  PubMed  Google Scholar 

  95. Ravelli G-P, Stein ZA, Susser MW . Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 1976; 295: 349–353.

    Article  CAS  PubMed  Google Scholar 

  96. Jones AP, Friedman MI . Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science 1982; 215: 1518–1519.

    Article  CAS  PubMed  Google Scholar 

  97. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD . Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol 2000; 279: E83–E87.

    CAS  Google Scholar 

  98. Hiremagalur BK, Vadlamudi S, Johanning GL, Patel MS . Long-term effects of feeding high carbohydrate diet in pre-weaning period by gastrostomy: a new rat model for obesity. Int J Obes Relat Metab Disord 1993; 17: 495–502.

    CAS  PubMed  Google Scholar 

  99. Enns MP, Wilson MW, Grinker JA, Faust IM, Jones AP, Friedman MI . Prenatal food restriction and subsequent weight gain in male rats. Science 1983; 219: 1093–1094.

    Article  CAS  PubMed  Google Scholar 

  100. Portha B, Kergoat M, Blondel O, Bailbe D . Underfeeding of rat mothers during the first two trimesters of gestation does not alter insulin action and insulin secretion in the progeny. Eur J Endocrinol 1995; 133: 475–482.

    Article  CAS  PubMed  Google Scholar 

  101. Ziegler E . Secular changes in the stature of adults and the secular trend of the modern sugar consumption. Z Kinderheilkd 1967; 99: 146–166.

    Article  CAS  PubMed  Google Scholar 

  102. Yudkin J . Sugar and disease. Nature 1972; 239: 197–199.

    Article  CAS  PubMed  Google Scholar 

  103. Putnam J, Allshouse J, Kantor LS . U.S. per capita food supply trends: more calories, refined carbohydrates and fats. Food Rev 2002; 25: 2–15.

    Google Scholar 

  104. Gross LS, Li L, Ford ES, Liu S . Increased consumption of refined carbohydrates and the epidemic of type 2 diabetes in the United States: an ecologic assessment. Am J Clin Nutr 2004; 79: 774–779.

    Article  CAS  PubMed  Google Scholar 

  105. Vallerand AL, Pérusse F, Bukowiecki LJ . Stimulatory effects of cold exposure and cold acclimation on glucose uptake in rat peripheral tissues. Am J Physiol 1990; 259: R1043–R1049.

    CAS  PubMed  Google Scholar 

  106. Haque MS, Minokoshi Y, Hamai M, Iwai M, Horiuchi M, Shimazu T . Role of the sympathetic nervous system and insulin in enhancing glucose uptake in peripheral tissues after intrahypothalamic injection of leptin in rats. Diabetes 1999; 48: 1706–1712.

    Article  CAS  PubMed  Google Scholar 

  107. Minokoshi Y, Kim Y-B, Peroni OD, Fryer LGD, Müller C, Carling D et al. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 2002; 415: 339–342.

    Article  CAS  PubMed  Google Scholar 

  108. Abe H, Minokoshi Y, Shimazu T . Effect of a β3-adrenergic agonist, BRL35135A, on glucose uptake in rat skeletal muscle in vivo and in vitro. J Endocrinol 1993; 139: 479–486.

    Article  CAS  PubMed  Google Scholar 

  109. Liu X, Pérusse F, Bukowiecki LJ . Chronic norepinephrine infusion stimulates glucose uptake in white and brown adipose tissues. Am J Physiol 1994; 266: R914–R920.

    CAS  PubMed  Google Scholar 

  110. Liu X, Pérusse F, Bukowiecki LJ . Mechanisms of the antidiabetic effects of the β3-adrenergic agonist CL-316243 in obese Zucker–ZDF rats. Am J Physiol 1998; 274: R1212–R1219.

    Article  CAS  PubMed  Google Scholar 

  111. Nikami H, Shimizu Y, Sumida M, Minokoshi Y, Yoshida T, Saito M et al. Expression of β3-adrenoceptor and stimulation of glucose transport by β3-agonists in brown adipocyte primary culture. J Biochem (Tokyo) 1996; 119: 120–125.

    Article  CAS  Google Scholar 

  112. Young JB . Programming of sympathoadrenal function. Trends Endocrinol Metab 2002; 13: 381–385.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

These studies were supported, in part, by USPHS Grant DK 20378.

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    J B Young

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Young, J. Developmental origins of obesity: a sympathoadrenal perspective. Int J Obes 30 (Suppl 4), S41–S49 (2006). https://doi.org/10.1038/sj.ijo.0803518

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