Hypothalamic control of hepatic lipid metabolism via the autonomic nervous system

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 28, Issue 5, 2014, Pages 673-684

  Bruinstroop, Eveline ^a   Fliers, Eric ^a   Kalsbeek, Andries ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

hypothalamus NPY autonomic nervous system arcuate nucleus VLDL TG

Indexed keywords

GLUCOSE; INSULIN; NEUROPEPTIDE Y; NORADRENALIN; PROOPIOMELANOCORTIN; LEPTIN;

ADRENERGIC SYSTEM; AUTONOMIC NERVOUS SYSTEM; CHOLINERGIC SYSTEM; DIET RESTRICTION; FEEDING; GENE EXPRESSION; HUMAN; HYPOTHALAMUS; LIPID METABOLISM; LIVER METABOLISM; NONHUMAN; REGULATORY MECHANISM; REVIEW; ANIMAL; ENERGY METABOLISM; LIVER; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; ENERGY METABOLISM; GLUCOSE; HUMANS; HYPOTHALAMUS; LEPTIN; LIPID METABOLISM; LIVER; NEURONS;

EID: 84924043381     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2014.05.001     Document Type: Review

References (87)

1. A.M. Strack, W.B. Sawyer, and J.H. Hughes A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections Brain Res 491 1989 156 162
2. S.E. La Fleur, A. Kalsbeek, and J. Wortel Polysynaptic neural pathways between the hypothalamus, including the suprachiasmatic nucleus, and the liver Brain Res 871 2000 50 56
3. R.M. Buijs, S.E. la Fleur, and J. Wortel The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons J Comp Neurol 464 2003 36 48
4. S. Stanley, S. Pinto, and J. Segal Identification of neuronal subpopulations that project from hypothalamus to both liver and adipose tissue polysynaptically Proc Natl Acad Sci U. S. A 107 2010 7024 7029
5. P.G. Luiten, G.J. ter Horst, and H. Karst The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord Brain Res 329 1985 374 378
6. P.G.M. Luiten, G.J. Ter Horst, and A.B. Steffens The hypothalamus, intrinsic connections and outflow pathways to the endocrine system in relation to the control of feeding and metabolism Prog Neurobiol 28 1987 1 54
7. N. Uyama, A. Geerts, and H. Reynaert Neural connections between the hypothalamus and the liver Anat Rec 280A 2004 808
8. A.D. Loewy Raphe pallidus and raphe obscurus projections to the intermediolateral cell column in the rat Brain Res 222 1981 129 133
9. A.D. Loewy, J.H. Wallach, and S. McKellar Efferent connections of the ventral medulla oblongata in the rat Brain Res 228 1981 63 80
10. R.S. McCuskey Anatomy of efferent hepatic nerves Anat Rec A Discov Mol Cell Evol Biol 280 2004 821 826
11. W.G. Forssmann, and S. Ito Hepatocyte innervation in primates J Cell Biol 74 1977 299 313
12. W. Metz, and W.G. Forssmann Innervation of the liver in guinea pig and rat Anat Embryol (Berl) 160 1980 239 252
13. Y. Fukuda, M. Imoto, and Y. Koyama Demonstration of noradrenaline-immunoreactive nerve fibres in the liver J Int Med Res 24 1996 466 472
14. G.F. Gibbons Assembly and secretion of hepatic very-low-density lipoprotein Biochem J 268 1990 1 13
15. T.M. Mason The role of factors that regulate the synthesis and secretion of very-low-density lipoprotein by hepatocytes Crit Rev Clin Lab Sci 35 1998 461 487
16. P. Nguyen, V. Leray, and M. Diez Liver lipid metabolism J Anim Physiol Anim Nutr (Berl) 92 2008 272 283
17. S. Otway, and D.S. Robinson The use of a non-ionic detergent (Triton WR 1339) to determine rates of triglyceride entry into the circulation of the rat under different physiological conditions J Physiol 190 1967 321 332
18. N. Zarjevski, I. Cusin, and R. Vettor Chronic intracerebroventricular neuropeptide-Y administration to normal rats mimics hormonal and metabolic changes of obesity Endocrinology 133 1993 1753 1758
19. K. Baran, E. Preston, and D. Wilks Chronic central melanocortin-4 receptor antagonism and central neuropeptide-Y infusion in rats produce increased adiposity by divergent pathways Diabetes 51 2002 152 158
20. S. Mashiko, A. Ishihara, and H. Iwaasa Characterization of neuropeptide Y (NPY) Y5 receptor-mediated obesity in mice: chronic intracerebroventricular infusion of D-Trp(34)NPY Endocrinology 144 2003 1793 1801
21. A. Sainsbury, I. Cusin, and F. Rohner-Jeanrenaud Adrenalectomy prevents the obesity syndrome produced by chronic central neuropeptide Y infusion in normal rats Diabetes 46 1997 209 214
22. K.E. Zakrzewska, A. Sainsbury, and I. Cusin Selective dependence of intracerebroventricular neuropeptide Y-elicited effects on central glucocorticoids Endocrinology 140 1999 3183 3187
23. C.X. Yi, E. Foppen, and W. Abplanalp Glucocorticoid signaling in the arcuate nucleus modulates hepatic insulin sensitivity Diabetes 61 2012 339 345
24. A.M. van den Hoek, P.J. Voshol, and B.N. Karnekamp Intracerebroventricular neuropeptide Y infusion precludes inhibition of glucose and VLDL production by insulin Diabetes 53 2004 2529 2534
25. J.M. Stafford, F. Yu, and R. Printz Central nervous system neuropeptide Y signaling modulates VLDL triglyceride secretion Diabetes 57 2008 1482 1490
26. M.M. Ollmann, B.D. Wilson, and Y.K. Yang Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein Science 278 1997 135 138
27. T. Adage, A.J.W. Scheurink, and S.F. De Boer Hypothalamic, metabolic, and behavioral responses to pharmacological inhibition of CNS melanocortin signaling in rats J Neurosci 21 2001 3639 3645
28. R. Nogueiras, P. Wiedmer, and D. Perez-Tilve The central melanocortin system directly controls peripheral lipid metabolism J Clin Invest 117 2007 3475 3488
29. B.H. Jones, J.H. Kim, and M.B. Zemel Upregulation of adipocyte metabolism by agouti protein: possible paracrine actions in yellow mouse obesity Am J Physiol 270 1996 E192 E196
30. N.J. Poritsanos, D. Wong, and M.E. Vrontakis Regulation of hepatic PPARgamma2 and lipogenic gene expression by melanocortin Biochem Biophys Res Commun 376 2008 384 388
31. D.C. Albarado, J. McClaine, and J.M. Stephens Impaired coordination of nutrient intake and substrate oxidation in melanocortin-4 receptor knockout mice Endocrinology 145 2004 243 252
32. J. Lin, Y.H. Choi, and D.L. Hartzell CNS melanocortin and leptin effects on stearoyl-CoA desaturase-1 and resistin expression Biochem Biophys Res Commun 311 2003 324 328
33. C.R. Barb, G.J. Hausman, and R. Rekaya Gene expression in hypothalamus, liver and adipose tissues and food intake response to melanocortin-4 receptor (MC4R) agonist in pigs expressing MC4R mutations Physiol Genom 41 2010 254 268
34. T.K. Lam, R. Gutierrez-Juarez, and A. Pocai Brain glucose metabolism controls the hepatic secretion of triglyceride-rich lipoproteins Nat Med 13 2007 171 180
35. T. Scherer, J. O'Hare, and K. Diggs-Andrews Brain insulin controls adipose tissue lipolysis and lipogenesis Cell Metab 13 2011 183 194
36. F.L. Tavares, and M.C. Seelaender Hepatic denervation impairs the assembly and secretion of VLDL-TAG Cell Biochem Funct 26 2008 557 565
37. F. Andreasen, P. Jakobsen, and H.J. Kornerup Changes in blood chemistry in hypertensive patients during propranolol therapy Br J Clin Pharmacol 17 1984 265 271
38. J.L. Day, J. Metcalfe, and C.N. Simpson Adrenergic mechanisms in control of plasma lipid concentrations Br Med J (Clin Res Ed) 284 1982 1145 1148
39. R. Fogari, A. Zoppi, and C. Pasotti Plasma lipids during chronic antihypertensive therapy with different beta-blockers J Cardiovasc Pharmacol 14 Suppl. 7 1989 S28 S32
40. J. Shaw, J.D. England, and A.S. Hua Beta-blockers and plasma triglycerides Br Med J 1 1978 986
41. M.C. Vinuela, and P.J. Larsen Identification of NPY-induced c-Fos expression in hypothalamic neurones projecting to the dorsal vagal complex and the lower thoracic spinal cord J Comp Neurol 438 2001 286 299
42. Y.C. Shi, J. Lau, and Z. Lin Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN Cell Metab 17 2013 236 248
43. J.M. Rojas, J.M. Stafford, and S. Saadat Central nervous system neuropeptide Y signaling via the Y1 receptor partially dissociates feeding behavior from lipoprotein metabolism in lean rats Am J Physiol Endocrinol Metab 303 2012 E1479 E1488
44. J. Kopp, Z.Q. Xu, and X. Zhang Expression of the neuropeptide Y Y1 receptor in the CNS of rat and of wild-type and Y1 receptor knock-out mice. Focus on immunohistochemical localization Neuroscience 111 2002 443 532
45. E. Bruinstroop, L. Pei, and M.T. Ackermans Hypothalamic neuropeptide Y (NPY) controls hepatic VLDL-triglyceride secretion in rats via the sympathetic nervous system Diabetes 61 2012 1043 1050
46. E. Bruinstroop, S.E. la Fleur, and M.T. Ackermans The autonomic nervous system regulates postprandial hepatic lipid metabolism Am J Physiol Endocrinol Metab 304 10 2013 E1089 E1096
47. G.P. Puschel Control of hepatocyte metabolism by sympathetic and parasympathetic hepatic nerves Anat Rec 280A 2004 854
48. A. Niijima Neural mechanisms in the control of blood glucose concentration J Nutr 119 1989 833 840
49. J.B. Young, and L. Landsberg Effect of diet and cold exposure on norepinephrine turnover in pancreas and liver Am J Physiol 236 1979 E524 E533
50. I.S. Racotta, R. Racotta, and L. Navarro Liver catecholamine turnover in fed and fasted rats estimated by synthesis and uptake blockade Horm Metab Res 26 1994 260 262
51. L. Landsberg Feast or famine: the sympathetic nervous system response to nutrient intake Cell Mol Neurobiol 26 2006 497 508
52. S.F. Morrison Differential control of sympathetic outflow Am J Physiol Regul Integr Comp Physiol 281 2001 R683 R698
53. R.M. Buijs, and F. Kreier The metabolic syndrome: a brain disease? J Neuroendocrinol 18 2006 715 716
54. R.H. Migliorini, M.A.R. Garofalo, and I.C. Kettelhut Increased sympathetic activity in rat white adipose tissue during prolonged fasting Am J Physiol 272 1997 R656 R661
55. T. Yamauchi, M. Iwai, and N. Kobayashi Noradrenaline and ATP decrease the secretion of triglyceride and apoprotein B from perfused rat liver Pflugers Arch 435 1998 368 374
56. T. Shimazu, and A. Fukuda Increased activities of glycogenolytic enzymes in liver after splanchnic-nerve stimulation Science 150 1965 1607 1608
57. F.R. Carreno, and M.C. Seelaender Liver denervation affects hepatocyte mitochondrial fatty acid transport capacity Cell Biochem Funct 22 2004 9 17
58. M. Miyazaki, Y.C. Kim, and M.P. Gray-Keller The biosynthesis of hepatic cholesterol esters and triglycerides is impaired in mice with a disruption of the gene for stearoyl-CoA desaturase 1 J Biol Chem 275 2000 30132 30138
59. W.W. Lautt, M.P. Macedo, and P. Sadri Hepatic parasympathetic (HISS) control of insulin sensitivity determined by feeding and fasting Am J Physiol 281 2001 G29 G36
60. L. Hodson, A.S. Bickerton, and S.E. McQuaid The contribution of splanchnic fat to VLDL triglyceride is greater in insulin-resistant than insulin-sensitive men and women: studies in the postprandial state Diabetes 56 2007 2433 2441
61. L.P. Klieverik, H.P. Sauerwein, and M.T. Ackermans Effects of thyrotoxicosis and selective hepatic autonomic denervation on hepatic glucose metabolism in rats Am J Physiol Endocrinol Metab 294 2008 E513 E520
62. K. Jungermann, A. Gardemann, and U. Beuers Regulation of liver metabolism by the hepatic nerves Adv Enzyme Regul 26 1987 63 88
63. C.M. Licht, S.A. Vreeburg, and A.K. van Reedt Dortland Increased sympathetic and decreased parasympathetic activity rather than changes in hypothalamic-pituitary-adrenal axis activity is associated with metabolic abnormalities J Clin Endocrinol Metab 95 2010 2458 2466
64. B. Beck, A. Burlet, and J.P. Nicolas Hypothalamic neuropeptide Y (NPY) in obese Zucker rats: implications in feeding and sexual behaviors Physiol Behav 47 1990 449 453
65. P.E. McKibbin, S.J. Cotton, and S. McMillan Altered neuropeptide Y concentrations in specific hypothalamic regions of obese (fa/fa) Zucker rats. Possible relationship to obesity and neuroendocrine disturbances Diabetes 40 1991 1423 1429
66. S. Dryden, L. Pickavance, and H.M. Frankish Increased neuropeptide Y secretion in the hypothalamic paraventricular nucleus of obese (fa/fa) Zucker rats Brain Res 690 1995 185 188
67. K.A. Takahashi, and R.D. Cone Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons Endocrinology 146 2005 1043 1047
68. R. Vettor, N. Zarjevski, and I. Cusin Induction and reversibility of an obesity syndrome by intracerebroventricular neuropeptide Y administration to normal rats Diabetologia 37 1994 1202 1208
69. B.D. White, and R.J. Martin Evidence for a central mechanism of obesity in the Zucker rat: role of neuropeptide Y and leptin Proc Exp Biol Med 214 1997 222 232
70. E. Parker, M. Van Heek, and A. Stamford Neuropeptide Y receptors as targets for anti-obesity drug development: perspective and current status Eur J Pharmacol 440 2002 173 187
71. N. Erondu, I. Gantz, and B. Musser Neuropeptide Y5 receptor antagonism does not induce clinically meaningful weight loss in overweight and obese adults Cell Metab 4 2006 275 282
72. E.M. Kim, E. OHare, and M.K. Grace ARC POMC mRNA and PVN alpha-MSH are lower in obese relative to lean Zucker rats Brain Res 862 2000 11 16
73. ATP channel subunit, Kir6.2, is associated with decreased expression of neuropeptide Y and agouti-related protein in the hypothalami of Zucker diabetic fatty rats J Neuroendocrinol 19 2007 941 951
74. D. Perez-Tilve, S.M. Hofmann, and J. Basford Melanocortin signaling in the CNS directly regulates circulating cholesterol Nat Neurosci 13 2010 877 882
75. G. Li, C.V. Mobbs, and P.J. Scarpace Central pro-opiomelanocortin gene delivery results in hypophagia, reduced visceral adiposity, and improved insulin sensitivity in genetically obese Zucker rats Diabetes 52 2003 1951 1957
76. M.D. Esler, H. Krum, and P.A. Sobotka Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial Lancet 376 2010 1903 1909
77. D.L. Bhatt, D.E. Kandzari, W.W. O'Neill SYMPLICITY HTN-3 Investigators A controlled trial of renal denervation for resistant hypertension N Engl J Med 370 2014 1393 1401
78. M.R. Carnethon, S.H. Golden, and A.R. Folsom Prospective investigation of autonomic nervous system function and the development of type 2 diabetes: the Atherosclerosis Risk in Communities study, 1987-1998 Circulation 107 2003 2190 2195
79. G. Grassi, R. Dell'Oro, and F. Quarti-Trevano Neuroadrenergic and reflex abnormalities in patients with metabolic syndrome Diabetologia 48 2005 1359 1365
80. N.E. Straznicky, M.T. Grima, and C.I. Sari Neuroadrenergic dysfunction along the diabetes continuum: a comparative study in obese metabolic syndrome subjects Diabetes 61 2012 2506 2516
81. J. Sobocki, G. Fourtanier, and J. Estany Does vagal nerve stimulation affect body composition and metabolism? Experimental study of a new potential technique in bariatric surgery Surgery 139 2006 209 216
82. D. Val-Laillet, A. Biraben, and G. Randuineau Chronic vagus nerve stimulation decreased weight gain, food consumption and sweet craving in adult obese minipigs Appetite 55 2010 245 252
83. J.G. Burneo, E. Faught, and R. Knowlton Weight loss associated with vagus nerve stimulation Neurology 59 2002 463 464
84. M.S. Koren, and M.D. Holmes Vagus nerve stimulation does not lead to significant changes in body weight in patients with epilepsy Epilepsy Behav 8 2006 246 249
85. U.N. Das Vagus nerve stimulation as a strategy to prevent and manage metabolic syndrome Med Hypothes 76 2011 429 433
86. J. Chen, P.J. Pasricha, and J. Yin Hepatic electrical stimulation reduces blood glucose in diabetic rats Neurogastroenterol Motil 22 2010 1109 1286
87. B. Finan, B. Yang, and N. Ottaway Targeted estrogen delivery reverses the metabolic syndrome Nat Med 18 2012 1847 1856