Stress- and diet-induced fat gain is controlled by NPY in catecholaminergic neurons

Molecular Metabolism

Volumn 3, Issue 5, 2014, Pages 581-591

  Zhang, Lei ^a,c   Lee, I Chieh J ^a   Enriquez, Rondaldo F ^a   Lau, Jackie ^a   Vähätalo, Laura H ^a   Baldock, Paul A ^a   Savontaus, Eriika ^b   Herzog, Herbert ^a,c  

^a ST VINCENT S HOSPITAL   (Australia)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Adiposity; Catecholaminergic neurons; Energy homeostasis; Neuropeptide Y; Stress

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; CARNITINE PALMITOYLTRANSFERASE I; CORTICOSTERONE; FATTY ACID SYNTHASE; GLUCOSE; INSULIN; NEUROPEPTIDE Y;

ADRENERGIC NERVE CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BODY COMPOSITION; BODY FAT; BODY TEMPERATURE; BROWN ADIPOSE TISSUE; CATECHOLAMINE NERVE CELL; CATECHOLAMINERGIC SYSTEM; CHRONIC STRESS; COLD STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENERGY BALANCE; ENZYME PHOSPHORYLATION; FAT GAIN; FAT MASS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; LIGHT DARK CYCLE; LIPID DIET; LIPOGENESIS; LUNG GAS EXCHANGE; MALE; MOUSE; NONHUMAN; NORADRENERGIC NERVE; OBESITY; PATHOGENESIS; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRESS; THERMOGENESIS; WEIGHT GAIN;

MUS;

EID: 84904317594     PISSN: 22128778     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.05.001     Document Type: Article

References (47)

1. Zhang L., Bijker M., Herzog H. The neuropeptide Y system: pathophysiological and therapeutic implications in obesity and cancer. Pharmacology & Therapeutics 2011, 131:91-113.
2. Kalra S.P., Kalra P.S. NPY and cohorts in regulating appetite, obesity and metabolic syndrome: beneficial effects of gene therapy. Neuropeptides 2004, 38:201-211.
3. Bai F.L., Yamano M., Shiotani Y., Emson P.C., Smith A.D., Powell J.F., et al. An arcuato-paraventricular and -dorsomedial hypothalamic neuropeptide Y-containing system which lacks noradrenaline in the rat. Brain Research 1985, 331:172-175.
4. Shi Y.C., Lau J., Lin Z., Zhang H., Zhai L., Sperk G., et al. Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metabolism 2013, 17:236-248.
5. Sawchenko P.E., Swanson L.W., Grzanna R., Howe P.R., Bloom S.R., Polak J.M. Colocalization of neuropeptide Y immunoreactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. Journal of Comparative Neurology 1985, 241:138-153.
6. Ekblad E., Edvinsson L., Wahlestedt C., Uddman R., Hakanson R., Sundler F. Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regulatory Peptides 1984, 8:225-235.
7. Gulbenkian S., Wharton J., Hacker G.W., Varndell I.M., Bloom S.R., Polak J.M. Co-localization of neuropeptide tyrosine (NPY) and its C-terminal flanking peptide (C-PON). Peptides 1985, 6:1237-1243.
8. Zukowska-Grojec Z., Neuropeptide Y. Anovel sympathetic stress hormone and more. Annals of the New York Academy of Sciences 1995, 771:219-233.
9. Kuo L.E., Czarnecka M., Kitlinska J.B., Tilan J.U., Kvetnansky R., Zukowska Z. Chronic stress, combined with a high-fat/high-sugar diet, shifts sympathetic signaling toward neuropeptide Y and leads to obesity and the metabolic syndrome. Annals of the New York Academy of Sciences 2008, 1148:232-237.
10. Ruohonen S.T., Pesonen U., Moritz N., Kaipio K., Roytta M., Koulu M., et al. Transgenic mice overexpressing neuropeptide Y in noradrenergic neurons: a novel model of increased adiposity and impaired glucose tolerance. Diabetes 2008, 57:1517-1525.
11. Ruohonen S.T., Vahatalo L.H., Savontaus E. Diet-induced obesity in mice overexpressing neuropeptide Y in noradrenergic neurons. International Journal of Peptides 2012, 2012. Article ID: 52524.
12. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience 2009, 10:397-409.
13. Karl T., Duffy L., Herzog H. Behavioural profile of a new mouse model for NPY deficiency. European Journal of Neuroscience 2008, 28:173-180.
14. Marks A., Vianna D.M., Carrive P. Nonshivering thermogenesis without interscapular brown adipose tissue involvement during conditioned fear in the rat. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2009, 296:R1239-R1247.
15. Sainsbury A., Schwarzer C., Couzens M., Fetissov S., Furtinger S., Jenkins A., et al. Important role of hypothalamic Y2 receptors in body weight regulation revealed in conditional knockout mice. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:8938-8943.
16. Zhang L., Macia L., Turner N., Enriquez R.F., Riepler S.J., Nguyen A.D., et al. Peripheral neuropeptide Y Y1 receptors regulate lipid oxidation and fat accretion. International Journal of Obesity (London) 2010, 34:357-373.
17. Kuo L.E., Kitlinska J.B., Tilan J.U., Li L., Baker S.B., Johnson M.D., et al. Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nature Medicine 2007, 13:803-811.
18. Ferrannini E. The theoretical bases of indirect calorimetry: a review. Metabolism 1988, 37:287-301.
19. Frayn K.N. Calculation of substrate oxidation rates invivo from gaseous exchange. Journal of Applied Physiology 1983, 55:628-634.
20. McLean J.A., Tobin G. Animal and human calorimetry 1987, Cambridge University Press, New York.
21. Young J.B., Saville E., Rothwell N.J., Stock M.J., Landsberg L. Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. Journal of Clinical Investigation 1982, 69:1061-1071.
22. Nedergaard J., Golozoubova V., Matthias A., Shabalina I., Ohba K., Ohlson K., et al. Life without UCP1: mitochondrial, cellular and organismal characteristics of the UCP1-ablated mice. Biochemical Society Transactions 2001, 29:756-763.
23. MacLean P.S., Higgins J.A., Johnson G.C., Fleming-Elder B.K., Peters J.C., Hill J.O. Metabolic adjustments with the development, treatment, and recurrence of obesity in obesity-prone rats. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2004, 287:R288-R297.
24. Saggerson E.D., Carpenter C.A. Carnitine palmitoyltransferase and carnitine octanoyltransferase activities in liver, kidney cortex, adipocyte, lactating mammary gland, skeletal muscle and heart. FEBS Letters 1981, 129:229-232.
25. McGarry J.D., Mills S.E., Long C.S., Foster D.W. Observations on the affinity for carnitine, and malonyl-CoA sensitivity, of carnitine palmitoyltransferase I in animal and human tissues. Demonstration of the presence of malonyl-CoA in non-hepatic tissues of the rat. Biochemical Journal 1983, 214:21-28.
26. Lin S., Storlien L.H., Huang X.F. Leptin receptor, NPY, POMC mRNA expression in the diet-induced obese mouse brain. Brain Research 2000, 875:89-95.
27. Bjorntorp P. Do stress reactions cause abdominal obesity and comorbidities?. Obesity Reviews 2001, 2:73-86.
28. Mikurube H., Kaneko M., Murata C., Komaki Y., Ishikawa N., Higashiyama R., et al. Association of change in the type of job with prevalence of components of the metabolic syndrome-special reference to job stress. Nihon Koshu Eisei Zasshi 2005, 52:987-993.
29. Bjorntorp P., Rosmond R. Hypothalamic origin of the metabolic syndrome X. Annals of the New York Academy of Sciences 1999, 892:297-307.
30. Bjorntorp P., Rosmond R. The metabolic syndrome - a neuroendocrine disorder?. British Journal of Nutrition 2000, 83(Suppl.1):S49-S57.
31. Black P.H. The inflammatory consequences of psychologic stress: relationship to insulin resistance, obesity, atherosclerosis and diabetes mellitus, type II. Medical Hypotheses 2006, 67:879-891.
32. Makimura H., Mizuno T.M., Roberts J., Silverstein J., Beasley J., Mobbs C.V. Adrenalectomy reverses obese phenotype and restores hypothalamic melanocortin tone in leptin-deficient ob/ob mice. Diabetes 2000, 49:1917-1923.
33. Nieuwenhuizen A.G., Rutters F. The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiology & Behavior 2008, 94:169-177.
34. Weaver J.U. Classical endocrine diseases causing obesity. Frontiers of Hormone Research 2008, 36:212-228.
35. Saito M., Bray G.A. Adrenalectomy and food restriction in the genetically obese (ob/ob) mouse. American Journal of Physiology 1984, 246:R20-R25.
36. Pralong F.P., Corder R., Gaillard R.C. The effects of chronic glucocorticoid excess, adrenalectomy and stress on neuropeptide Y in individual rat hypothalamic nuclei. Neuropeptides 1993, 25:223-231.
37. Fuzesi T., Wittmann G., Liposits Z., Lechan R.M., Fekete C. Contribution of noradrenergic and adrenergic cell groups of the brainstem and agouti-related protein-synthesizing neurons of the arcuate nucleus to neuropeptide-Y innervation of corticotropin-releasing hormone neurons in hypothalamic paraventricular nucleus of the rat. Endocrinology 2007, 148:5442-5450.
38. Liposits Z., Sievers L., Paull W.K. Neuropeptide-Y and ACTH-immunoreactive innervation of corticotropin releasing factor (CRF)-synthesizing neurons in the hypothalamus of the rat. An immunocytochemical analysis at the light and electron microscopic levels. Histochemistry 1988, 88:227-234.
39. Forbes S., Herzog H., Cox H.M. Arole for neuropeptide Y in the gender-specific gastrointestinal, corticosterone and feeding responses to stress. British Journal of Pharmacology 2012, 166:2307-2316.
40. Ruderman N.B., Saha A.K., Kraegen E. Minireview: malonyl CoA, AMP-activated protein kinase, and adiposity. Endocrinology 2003, 144:5166-5171.
41. Brownsey R.W., Boone A.N., Elliott J.E., Kulpa J.E., Lee W.M. Regulation of acetyl-CoA carboxylase. Biochemical Society Transactions 2006, 34:223-227.
42. Wang J.T., Xu S.W. Effects of cold stress on the messenger ribonucleic acid levels of corticotrophin-releasing hormone and thyrotropin-releasing hormone in hypothalami of broilers. Poultry Science 2008, 87:973-978.
43. Helmreich D.L., Parfitt D.B., Lu X.Y., Akil H., Watson S.J. Relation between the hypothalamic-pituitary-thyroid (HPT) axis and the hypothalamic-pituitary-adrenal (HPA) axis during repeated stress. Neuroendocrinology 2005, 81:183-192.
44. van den Hoek A.M., Voshol P.J., Karnekamp B.N., Buijs R.M., Romijn J.A., Havekes L.M., et al. Intracerebroventricular neuropeptide Y infusion precludes inhibition of glucose and VLDL production by insulin. Diabetes 2004, 53:2529-2534.
45. Marks J.L., Waite K. Intracerebroventricular neuropeptide Y acutely influences glucose metabolism and insulin sensitivity in the rat. Journal of Neuroendocrinology 1997, 9:99-103.
46. Marks J.L., Waite K. Some acute effects of intracerebroventricular neuropeptide Y on insulin secretion and glucose metabolism in the rat. Journal of Neuroendocrinology 1996, 8:507-513.
47. van den Hoek A.M., van Heijningen C., Schroder-van der Elst J.P., Ouwens D.M., Havekes L.M., Romijn J.A., et al. Intracerebroventricular administration of neuropeptide Y induces hepatic insulin resistance via sympathetic innervation. Diabetes 2008, 10:10.