If body fatness is under physiological regulation, then how come we have an obesity epidemic?

Physiology

Volumn 29, Issue 2, 2014, Pages 88-98

  Speakman, John R ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ADIPOSE TISSUE; ANIMAL; EATING; HUMAN; METABOLISM; OBESITY; THEORETICAL MODEL;

ADIPOSE TISSUE; ANIMALS; EATING; HUMANS; MODELS, THEORETICAL; OBESITY; PROTEINS;

EID: 84900810507     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00053.2013     Document Type: Review

References (86)

1. Ahima RS, Prabakaran D, Mantzoros C, Qu DQ, Lowell B, Maratos-Flier E, Flier JS. Role of leptin in the neuroendocrine response to fasting. Nature 382: 250-252, 1996.
2. Asakawa A, Inui A, Yuzuriha H, Ueno N, Katsura G, Fujimiya M, Fujino MA, Niijima A, Meguid MM, Kasuga M. Characterization of the effects of pancreatic polypeptide in the regulation of energy balance. Gastroenterology 124: 1325-1336, 2003.
3. Badman MK, Flier JS. The gut and energy balance: visceral allies in the obesity wars. Science 307: 1909-1914, 2005.
4. Bartness TJ, Keen-Rhinehart E, Dailey MJ, Teubner BJ. Neural and hormonal control of food hoarding. Am J Physiol Regul Integr Comp Physiol 301: R641-R655, 2011.
5. Blundell JE, Caudwell P, Gibbons C, Hopkins M, Naslund E, King NA, Finlayson G. Body composition and appetite: fat-free mass (but not fat mass or BMI) is positively associated with self-determined meal size and daily energy intake in humans. Br J Nutr 107: 445-449, 2012.
6. Blundell JE, Caudwell P, Gibbons C, Hopkins M, Naslund E, King NA, Finlayson G. Role of resting metabolic rate and energy expenditure in hunger and appetite control: a new formulation. Disease Models Mechanisms 5: 608-613, 2012.
7. Boutin S. Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68: 203-220, 1990.
8. Brain CK. The Hunters or the Hunted? An Introduction to African Cave Taphonomy. Chicago, IL: Univ. of Chicago Press, 1981.
9. Brodin A. Mass-dependent predation and metabolic expenditure in wintering birds: Is there a trade-off between different forms of predation? Animal Behav 62: 993-999, 2001.
10. Carlsen M, Lodal J, Leirs H, Jensen TS. The effect of predation risk on body weight in the field vole, Microtus agrestis. Oikos 87: 277-285, 1999.
11. Chakravarthy MV, Booth FW. Eating, exercise, and "thrifty" genotypes: connecting the dots toward an evolutionary understanding of modern chronic diseases. J Appl Physiol 96: 3-10, 2004.
12. Chance WT, Balasubramaniam A, Stallion A, Fischer JE. Anorexia following the systemic injection of amylin. Brain Res 607: 185-188, 1993.
13. Chaudhri OB, Salem V, Murphy KG, Bloom SR. Gastrointestinal satiety signals. Annu Rev Physiol 70: 239-255, 2008.
14. Claret M, Smith MA, Batterham RL, Selman C, Choudhury AI, Fryer LGD, Clements M, Al-Qassab H, Heffron H, Xu AW, Speakman JR, Barsh GS, Viollet B, Vaulont S, Ashford MLJ, Carling D, Withers DJ. AMPK is essential for energy homeostasis regulation and glucosesensing by POMC and AgRP Neurons. J Clin Invest 117: 2325-2336, 2007.
15. Cowley MA, Smith RG, Diano S, Tschop M, Pron-chuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heinman ML, Garcia-Segura LM, Nillni EA, et al. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy ho-meostasis. Neuron 37: 649-661, 2003.
16. Cummings DE, Overduin J. Gastrointestinal regulation of food intake. J Clin Invest 117: 13-23, 2007.
17. Di Marzo V, Ligresti A, ad Cristino L. The endo-cannabinoid system as a link between homoeo-static and hedonic pathways involved in energy balance regulation. Intl J Obesity 33: 18-24, 2009.
18. Eknoyan G. A history of obesity, or how what was good became ugly and then bad. Adv Chronic Kidney Dis 13: 421-427, 2006.
19. Eller E, Hawks J, Relethford JH. Local extinction and recolonisation, species effective population size and modern human origins. Hum Biol 81: 805-824, 2009.
20. Flegal KM, et al. Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303: 235-241, 2010.
21. Flegal KM, Shepherd JA, Looker CA, et al. Overweight and obesity in the united states: prevalence and trends 1960-1994. Intl J Obesity 22: 39-47, 1998.
22. Fletcher QE, Landry-Cuerrier M, Boutin S, Mc-Adam AG, Speakman JR, Humphries MM. Reproductive timing and reliance on hoarded capital resources by lactating red squirrels. Oecologia (Berl) 173: 1203-1215, 2013.
23. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature 395: 763-770, 1998.
24. Gosler AG, Greenwood JJD, Perrins C. Predation risk and the cost of being fat. Nature 377: 621-623, 1995.
25. Gulati P, Cheung MK, Antrobus R, Church CD, Harding HP, Tung YCL, Rimmington D, Ma M, Ron D, et al. Role for the obesity-related FTO gene in the cellular sensing of amino acids. PNAS 110: 2557-2562, 2013.
26. Harding RM, Fullerton SM, Griffiths RC, Bond J, Cox MJ, Schneider JA, Moulin DS, Clegg JB. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am J Hum Genet 60: 772-789, 1997.
27. Heisler LK, Jobst EE, Sutton GM, Zhou LG, Borok E, Thornton-Jones Z, Liu HY, Zigman JM, Balthasa R, Kishi T, Lee CE, et al. Serotonin reciprocally regulates melanocortin neurons to modulate food intake. Neuron 51: 239-249, 2006.
28. Heymsfield SB, Greenberg AS, Fujioka K, Dixon RM, Kushner R, Hunt T, Lubina JA, Patane J, Self B, Hunt P, et al. Recombinant leptin for weight loss in obese and lean adults: a randomized, controlled, dose-escalation trial. JAMA 282: 1569-1575, 1999.
29. Higginson AD, McNamara JM, Houston AI. The Starvation-predation trade-off predicts trends in body size, muscularity, and adiposity between and within taxa. Am Nat 179: 338-350, 2012.
30. Huang X, Hancock DP, Gosby AK, McMahin AC, Solon SMC, Le Couteur DG, Conigrave AD, Raubenheimer D, Simpson SJ. Effects of dietary protein to carbohydrate balance on energy intake, fat storage, and heat production in mice. Obesity (Silver Spring) 21: 85-92, 2013.
31. Hussain SS, Bloom SR. The regulation of food intake by the gut-brain axis: implications for obesity. Intl J Obesity 37: 625-633, 2013.
32. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, et al. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104: 15069-15074, 2007.
33. Johnson MS, Thomson SC, Speakman JR. Limits to sustained energy intake I. Lactation in the laboratory mouse Mus musculus. J Exp Biol 204: 1925-1935, 2001.
34. Johnson RJ, Steinvinkel P, Martin SL, Jani A, San-chez-Lozada LG, Hill JO, Lanaspa MA. Redefining metabolic syndrome as a fat storage condition based on studies of comparative physiology. Obesity (Silver Spring) 21: 659-664, 2013.
35. Kaiyala KJ, Morton GJ, Thaler JP, Meek TH, Tylee T, Ogimoto K, Wisse BE. Acutely decreased ther-moregulatory energy expenditure or decreased activity energy expenditure both acutely reduce food intake in mice. PLos One 7: e41473, 2012.
36. Kenny PJ. Reward mechanisms in obesity: new insights and future directions. Neuron 69: 664-679, 2011.
37. Koch CE, Goddeke S, Kruger M, Tups A. Effect of central and peripheral leucine on energy metabolism in the Djungarian hamster (Phodopus sun-gorus). J Comp Physiol B 183: 261-268, 2013.
38. Kojima M, Hosada H, Date Y, Nakazoto M, Mat-suo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402: 656-660, 1999.
39. Kumar KG, Trevaskis JL, Lam DD, Sutton GM, Koza RA, Chouljenko VN, Kousoulas KG, Rogers PM, Kesterson RA, Thearle M, Ferrante AW, My-natt RL, et al. Identification of adropin as a secreted factor linking dietary macronutrient intake with energy homeostasis and lipid metabolism. Cell Metab 8: 468-481, 2008.
40. Lenard NR, Berthoud HR. Central and peripheral regulation of food intake and physical activity: pathways and genes. Obesity 16, Suppl 3: S11-S22, 2008.
41. Lev-Ran A. Human obesity: an evolutionary approach to understanding our bulging waistline. Diabetes Metab Res Rev 17: 347-362, 2001.
42. Levitsky DA. Putting behavior back into feeding behavior: a tribute to George Collier. Appetite 38: 143-148, 2002.
43. Lima SL. Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology 67: 377-385, 1986.
44. Liu YL, Semjonous NM, Murphy KG, Ghatei MA, Bloom SR. The effects of pancreatic polypeptide on locomotor activity and food intake in mice. Intl J Obesity 32: 1712-1715, 2008.
45. MacLeod R, MacLeod CD, Learmouth JA, Jepson PD, Reid RJ, Deaville R, Pierce GJ. Mass-dependent predation risk in lethal dolphin porpoise interactions. Proc Roy Soc B 274: 2587-2593, 2007.
46. Mizuno TM. Interaction between leptin and gut hormones in the regulation of food intake and body weight. In: Leptin, Hormonal Dysfunctions and Clinical Yses, edited by Hemling RM, Belkin AT. Hauppauge, NY: Nova Science Publishers, 2011.
47. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight. Nature 443: 289-295, 2006.
48. Murphy KG, Bloom SR. Gut hormones and the regulation of energy homeostasis. Nature 444: 854-859, 2006.
49. Nakazato M, Murikami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S. A role for Ghrelin in the central regulation of feeding. Nature 409: 194-198, 2001.
50. Neel JV. Diabetes mellitus a 'thrifty' genotype rendered detrimental by 'progress'? Am J Hum Genet 14: 352-353, 1962.
51. Parker JA, Bloom SR. Hypothalamic neuropep-tides and the regulation of appetite. Neurophar-macology 63: S1, 18-30, 2012.
52. Perello M, Raingo J. Leptin activates oxytocin neurons of the hypothalamic paraventricular nucleus in both control and diet-induced obese rodents. PLos One 8: e59625, 2013.
53. Perry B, Wang Y. Appetite regulation and weight control: the role of gut hormones. Nutr Diabetes 2: e26, 2012.
54. Pickering TR, Clarke RJ, Moggi-Cecchi J. Role of carnivores in the accumulation of the Sterkfon-tein Member 4 hominid assemblage: a tapho-nomic reassessment of the complete hominid fossil sample (1936-1999). Am J Phys Anthropol 125: 1-15, 2004.
55. Porte D, Baskin DG, Schwartz MW. Leptin and insulin action in the central nervous system. Nutr Rev 60: S20-S29, 2002.
56. Prentice AM. Obesity and its potential mechanistic basis. Br Med Bull 60: 51-67, 2001.
57. Prentice AM. Early influences on human energy regulation: thrifty genotypes and thrifty pheno-types. Physiol Behav 86: 640-645, 2005.
58. Prentice AM, Rayco-Solon P, Moore SE. Insights from the developing world: thrifty genotypes and thrifty phenotypes. Proc Nutr Soc 64: 153-161, 2005.
59. Sam AH, Troke RC, Tan TM, Bewick GA. The role of the gut/brain axis in modulating food intake. Neuropharmacol 63: S1, 46-56, 2012.
60. Schwartz MW, Woods SC, Porte D, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661-671, 2000.
61. Schwartz MW, Woods SC, Seeley RJ, Barsh GS, Baskin DG, Leibel RL. Is the energy homeostasis system inherently biased toward weight gain? Diabetes 52: 232-238, 2003.
62. Shin AC, Zheng HY, Berthoud HR. An expanded view of energy homeostasis: neural integration of metabolic, cognitive, and emotional drives to eat. Physiol Behav 97: 572-580, 2009.
63. Shioda S, Kageyama H, Takenoya F, Shiba K. Galanin-like peptide: a key player in the homeo-static regulation of feeding and energy metabolism? Intl J Obesity 35: 619-628, 2011.
64. Simpson SJ, Raubenheimer D. Obesity: the protein leverage hypothesis. Obes Rev 6: 133-142, 2005.
65. Song B, Thomas DM. Dynamics of starvation in humans. J Math Biol 54: 27-43, 2007.
66. Sorensen A, Mayntz D, Raubenheimer D, Simpson SJ. Protein-leverage in mice: the geometry of macronutrient balancing and consequences for fat deposition. Obesity (Silver Spring) 16: 566-571, 2008.
67. Speakman JR. A novel non-adaptive scenario explaining the genetic pre-disposition to obesity: the 'predation release' hypothesis. Cell Metab 6: 5-11, 2007.
68. Speakman JR. Thrifty genes for obesity and diabetes, an attractive but flawed idea and an alternative scenario: the 'drifty gene' hypothesis. Intl J Obesity 32: 1611-1617, 2008.
69. Speakman JR, Krol E. Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79: 726-746, 2010.
70. Speakman JR, Levitsky DA, Allison DB, Bray MS, de Castro JM, Clegg DJ, Clapham JC, Dulloo AG, Gruer L, Haw S, Hebebrand J, Hetherington MM, et al. Set-points, settling points and some alternative models: theoretical options to understand how genes and environments combine to regulate body adiposity. Dis Models Mechan 4: 733-745, 2011.
71. Speakman JR, Westerterp KR. A mathematical model of weight loss under total starvation: evidence against the thrifty-gene hypothesis. Dis Models Mechan 6: 236-251, 2013.
72. Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Allen HL, Lindgren CM, Luan J, Mägi R, et al. Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nature Genetics 42: 937-948, 2010.
73. Tong QC, Ye CP, Jones JE, Elmquist JK, Lowell BB. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nature Neurosci 11: 998-1000, 2008.
74. Tschop M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 407: 908-913, 2000.
75. Volkow ND, Wang GJ, Baler RD. Reward, dopa-mine and the control of food intake: implications for obesity. Trends Cognitive Sci 15: 37-46, 2011.
76. Vucetic Z, Reyes TM. Central dopaminergic circuitry controlling food intake and reward: implications for the regulation of obesity. Wiley Interdisciplinary Rev Systems Biol Med 2: 577-593, 2010.
77. Watnick S. Obesity: a problem of Darwinian proportions? Ad Chron Kid Dis 13: 428-432, 2006.
78. Wells JCK. The evolution of human fatness and susceptibility to obesity: an ethological approach. Biol Rev 81: 183-205, 2006.
79. Werner L, Muller-Fielitz H, Ritzal M, Werner T, Rossner M, Schwaninger M. Involvement of dou-blecortin-expressing cells in the arcuate nucleus in body weight regulation. Endocrinology 153: 2655-2664, 2012.
80. Willer CJ, Speliotes EK, Loos RJF, et al. Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nature Genetics 41: 25-35, 2009.
81. Woods SC, Seeley RJ, Porte D, Schwartz MW. Signals that regulate food intake and energy ho-meostasis. Science 280: 1378-1383, 1998.
82. Woods SC, Seeley RJ, Porte D, Schwartz MW. Food intake and the regulation of body weight. Ann Rev Physiol 51: 255-277, 2000.
83. Xu Y, Jones JE, Kohno D, Williams KW, Lee CE, Choi MJ, Anderson JG, Heisler LK, Zigman JM, Lowell BB, Elmquist JK. 5-HT(2C)Rs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 60: 582-589, 2008.
84. Xu YZ, O'Brien WG, Lee CC, Myers MG, Tong QC. Role of GABA release from leptin receptor-expressing neurons in body weight regulation. Endocrinology 153: 2223-2233, 2012.
85. Young AA. Brainstem sensing of meal related signals in energy homeostasis. Neuropharmacol-ogy 63: S1, 31-45, 2012.
86. Zhang YY, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homolog. Nature 372: 425-432, 1994.