A temperature hypothesis of hypothalamus-driven obesity

Yale Journal of Biology and Medicine

Volumn 87, Issue 2, 2014, Pages 149-158

  Horvath, Tamas L ^a,b,c   Stachenfeldd, Nina S ^c,d   Diano, Sabrina ^a,b,c  

^a Cell Signaling and Neurobiology of Metabolism ^*  (United States)

^b Section of Comparative Medicine   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHN B PIERCE LABORATORY   (United States)

Author keywords

Circuit activity; Hypothalamus; Obesity; Temperature regulation

Indexed keywords

ARTICLE; BRAIN METABOLISM; BRAIN TEMPERATURE; CORE TEMPERATURE; FEEDING; HUMAN; HYPOTHALAMUS; HYPOTHESIS; METABOLIC REGULATION; NONHUMAN; OBESITY; PEPTIDERGIC NERVOUS SYSTEM; THERMOREGULATION; ANIMAL; BIOLOGICAL MODEL; BODY TEMPERATURE; FEEDING BEHAVIOR; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BODY TEMPERATURE; FEEDING BEHAVIOR; HUMANS; HYPOTHALAMUS; MODELS, BIOLOGICAL; OBESITY;

EID: 84902118909     PISSN: 00440086     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Brobeck JR. Mechanism of the development of obesity in animals with hypothalamic lesions. Physiol Rev. 1946;26(4):541-59.
2. Strominger JL, Brobeck JR. A mechanism of regulation of food intake. Yale J Biol Med. 1953;25(5):383-90.
3. Leibel RL, Chung WK, Chua SC, Jr. The molecular genetics of rodent single gene obesities. J Biol Chem. 1997;272(51):31937-40.
4. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature. 1998;395(6704):763-70.
5. Elmquist JK, Elias CF, Saper CB. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron. 1999;22(2):221-32.
6. Gao Q, Horvath TL. Neurobiology of feeding and energy expenditure. Annu Rev Neurosci. 2007;30:367-98.
7. Myers MG, Jr., Olson DP. Central nervous system control of metabolism. Nature. 2012;491(7424):357-63.
8. Seeley RJ, Woods SC. Monitoring of stored and available fuel by the CNS: implications for obesity. Nat Rev Neurosci. 2003;4(11):901-9.
9. Horvath TL, Diano S, Tschop M. Brain circuits regulating energy homeostasis. Neuroscientist. 2004;10(3):235-46.
10. Sherrington C. Cutaneous Sensation. In: Sharpey-Schäfer EA, editor. Text-book of physiology. Edinburgh: YJ Pentland; 1898. p. 920-1001.
11. Cannon WB, Washburn AL. An explanation of hunger. 1911. Obes Res. 1993;1(6):494-500.
12. Carlson AJ. The control of hunger in health and disease. Chicago: The University of Chicago Press; 1916.
13. Hetherington AW, Ranson SW. The relation of various hypothalamic lesions to adiposity in the rat. J Comp Neurol. 1942;76(3):475-99.
14. Hetherington AW. Non-production of hypothalamic obesity in the rat by lesions rostral or dorsal to the ventro-medial hypothalamic nuclei. J Comp Neurol. 1944;80(1):33-45.
15. Anand BK, Brobeck JR. Hypothalamic control of food intake in rats and cats. Yale J Biol Med. 1951;24(2):123-40.
16. Hetherington AW. The relation of various hypothalamic lesions to adiposity and other phenomena in the rat. Am J Physiol. 1941;133:326.
17. Coleman DL. Diabetes-obesity syndromes in mice. Diabetes. 1982;31(Suppl 1 Pt 2):1-6.
18. Zucker LM, Zucker TF. Fatty, a new mutation in the rat. Journal of Heredity. 1961;52(6):275-8.
19. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372(6505):425-32.
20. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, et al. Weightreducing effects of the plasma protein encoded by the obese gene. Science. 1995;269(5223):543-6.
21. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 1995;269(5223):540-3.
22. Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science. 1995;269(5223):546-9.
23. Mercer JG, Hoggard N, Williams LM, Lawrence CB, Hannah LT, Trayhurn P. Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization. FEBS Lett. 1996;387(2-3):113-6.
24. Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG. Identification of targets of leptin action in rat hypothalamus. J Clin Invest. 1996;98(5):1101-6.
25. Mountjoy KG, Robbins LS, Mortrud MT, Cone RD. The cloning of a family of genes that encode the melanocortin receptors. Science. 1992;257(5074):1248-51.
26. Robbins LS, Nadeau JH, Johnson KR, Kelly MA, Roselli-Rehfuss L, Baack E, et al. Pigmentation phenotypes of variant extension locus alleles result from point mutations that alter MSH receptor function. Cell. 1993;72(6):827-34.
27. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, et al. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell. 1997;88(1):131-41.
28. Pelletier G, Dube D. Electron microscopic immunohistochemical localization of alpha-msh in the rat brain. Am J Anat. 1977;150(1):201-5.
29. Seeley RJ, Yagaloff KA, Fisher SL, Burn P, Thiele TE, van Dijk G, et al. Melanocortin receptors in leptin effects. Nature. 1997;390(6658):349.
30. Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, Gantz I, et al. Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science. 1997;278(5335):135-8.
31. Hahn TM, Breininger JF, Baskin DG, Schwartz MW. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci. 1998;1(4):271-2.
32. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, et al. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron. 1999;23(4):775-86.
33. Cowley MA, Smart JL, Rubinstein M, Cerdan MG, Diano S, Horvath TL, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 2001;411(6836):480-4.
34. Horvath TL, Naftolin F, Kalra SP, Leranth C. Neuropeptide-Y innervation of beta-endorphin-containing cells in the rat mediobasal hypothalamus: a light and electron microscopic double immunostaining analysis. Endocrinology. 1992;131(5):2461-7.
35. Stephens TW, Basinski M, Bristow PK, Bue-Valleskey JM, Burgett SG, Craft L, et al. The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature. 1995;377(6549):530-2.
36. Thornton JE, Cheung CC, Clifton DK, Steiner RA. Regulation of hypothalamic proopiomelanocortin mRNA by leptin in ob/ob mice. Endocrinology. 1997;138(11):5063-6.
37. Spanswick D, Smith MA, Mirshamsi S, Routh VH, Ashford ML. Insulin activates ATP-sensitive K+ channels in hypothalamic neurons of lean, but not obese rats. Nat Neurosci. 2000;3(8):757-8.
38. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, et al. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature. 2002;418(6898):650-4.
39. Barsh GS, Schwartz MW. Genetic approaches to studying energy balance: perception and integration. Nat Rev Genet. 2002;3(8):589-600.
40. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, et al. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science. 2004;304(5667):110-5.
41. Schally AV, Kastin AJ, Arimura A, Coy D, Coy E, Debeljuk L, et al. Basic and clinical studies with luteinizing hormone-releasing hormone (LH-RH) and its analogues. J Reprod Fertil Suppl. 1973;20(0):119-36.
42. Pfaff DW, Schwanzel-Fukuda M, Parhar IS, Lauber AH, McCarthy LM, Kow LM. GnRH neurons and other cellular and molecular mechanisms for simple mammalian reproductive behaviors. Recent Prog Horm Res. 1994;49:1-25.
43. Tilly JL, Kolesnick RN. Realizing the promise of apoptosis-based therapies: separating the living from the clinically undead. Cell Death Differ. 2003;10(5):493-5.
44. Brobeck JR. Neural control of hunger, appetite, and satiety. Yale J Biol Med. 1957;29(6):565-74.
45. Nielsen B, Astrup A, Samuelsen P, Wengholt H, Christensen NJ. Effect of physical training on thermogenic responses to cold and ephedrine in obesity. Int J Obes Relat Metab Disord. 1993;17(7):383-90.
46. Emmett JD. A review of heart rate and blood pressure responses in the cold in healthy subjects and coronary artery disease patients. J Cardiopulm Rehabil. 1995;15(1):19-24.
47. Granberg PO. Human physiology under cold exposure. Arctic Med Res. 1991;50(Suppl 6):23-7.
48. Matsumoto T, Miyawaki T, Ue H, Kanda T, Zenji C, Moritani T. Autonomic responsiveness to acute cold exposure in obese and nonobese young women. Int J Obes Relat Metab Disord. 1999;23(8):793-800.
49. Stocks JM, Taylor NA, Tipton MJ, Greenleaf JE. Human physiological responses to cold exposure. Aviat Space Environ Med. 2004;75(5):444-57.
50. Mekjavic IB, Eiken O. Inhibition of shivering in man by thermal stimulation of the facial area. Acta Physiol Scand. 1985;125(4):633-7.
51. Frank SM, Higgins MS, Fleisher LA, Sitzmann JV, Raff H, Breslow MJ. Adrenergic, respiratory, and cardiovascular effects of core cooling in humans. Am J Physiol. 1997;272(2 Pt 2):R557-62.
52. Nakajima Y, Takamata A, Ito T, Sessler DI, Kitamura Y, Shimosato G, et al. Upright posture reduces thermogenesis and augments core hypothermia. Anesth Analg. 2002;94(6):1646-51, table of contents.
53. Horvath TL, Diano S, van den Pol AN. Synaptic interaction between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J Neurosci. 1999;19(3):1072-87.
54. Coppola A, Liu ZW, Andrews ZB, Paradis E, Roy MC, Friedman JM, et al. A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab. 2007;5(1):21-33.
55. Andrews ZB, Liu ZW, Walllingford N, Erion DM, Borok E, Friedman JM, et al. UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals. Nature. 2008;454(7206):846-51.
56. Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO, et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest. 2012;122(1):153-62.
57. Diano S, Liu ZW, Jeong JK, Dietrich MO, Ruan HB, Kim E, et al. Peroxisome proliferation-associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat Med. 2011;17(9):1121-7.
58. Dietrich MO, Liu ZW, Horvath TL. Mitochondrial dynamics controlled by mitofusins regulate Agrp neuronal activity and diet-induced obesity. Cell. 2013;155(1):188-99.
59. Schneeberger M, Dietrich MO, Sebastian D, Imbernon M, Castano C, Garcia A, et al. Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell. 2013;155(1):172-87.
60. Ozcan U. Mitofusins: mighty regulators of metabolism. Cell. 2013;155(1):17-8.
61. Halliday D, Hesp R, Stalley SF, Warwick P, Altman DG, Garrow JS. Resting metabolic rate, weight, surface area and body composition in obese women. Int J Obes. 1979;3(1):1-6.
62. Bogardus C, Lillioja S, Ravussin E, Abbott W, Zawadzki JK, Young A, et al. Familial dependence of the resting metabolic rate. N Engl J Med. 1986;315(2):96-100.
63. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986;78(6):1568-78.
64. Toner MM, Sawka MN, Pandolf KB. Thermal responses during arm and leg and combined arm-leg exercise in water. J Appl Physiol Respir Environ Exerc Physiol. 1984;56(5):1355-60.
65. Veicsteinas A, Ferretti G, Rennie DW. Superficial shell insulation in resting and exercising men in cold water. J Appl Physiol Respir Environ Exerc Physiol. 1982;52(6):1557-64.
66. Jequier E, Gygax PH, Pittet P, Vannotti A. Increased thermal body insulation: relationship to the development of obesity. J Appl Physiol. 1974;36(6):674-8.
67. Vallerand AL, Zamecnik J, Jacobs I. Plasma glucose turnover during cold stress in humans. J Appl Physiol (1985). 1995;78(4):1296-302.
68. Yeckel CW, Taksali SE, Dziura J, Weiss R, Burgert TS, Sherwin RS, et al. The normal glucose tolerance continuum in obese youth: evidence for impaierment in beta-cell function independent of insulin resistance. J Clin Endocrinol Metab. 2005;90(2):747-54.
69. Kasai T, Hirose M, Matsukawa T, Takamata A, Yaegashi K, Tanaka Y. Preoperative blood pressure and catecholamines related to hypothermia during general anesthesia. Acta Anaesthesiol Scand. 2003;47(2):208-12.
70. Ravussin E, Lillioja S, Knowler WC, Christin L, Freymond D, Abbott WG, et al. Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med. 1988;318(8):467-72.
71. Rising R, Keys A, Ravussin E, Bogardus C. Concomitant interindividual variation in body temperature and metabolic rate. Am J Physiol. 1992;263(4 Pt 1):E730-4.
72. Tataranni PA, Young JB, Bogardus C, Ravussin E. A low sympathoadrenal activity is associated with body weight gain and development of central adiposity in Pima Indian men. Obes Res. 1997;5(4):341-7.
73. Bray GA, York DA, Fisler JS. Experimental obesity: a homeostatic failure due to defective nutrient stimulation of the sympathetic nervous system. Vitam Horm. 1989;45:1-125.