Short term voluntary overfeeding disrupts brain insulin control of adipose tissue lipolysis

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 33061-33069

  Scherer, Thomas ^a,b   Lindtner, Claudia ^a   Zielinski, Elizabeth ^a   O'Hare, James ^a   Filatova, Nika ^a   Buettner, Christoph ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTES; ADIPOSE TISSUE; ENDOCANNABINOID; GLUCOSE FLUX; GLUCOSE PRODUCTION; HIGH-FAT DIET; HUMAN OBESITY; INSULIN RESISTANCE; INSULIN SIGNALING; SHORT TERM; SPRAGUE-DAWLEY RATS; SYMPATHETIC NERVOUS SYSTEMS; TYPE-2 DIABETES; WHITE ADIPOSE TISSUES;

BRAIN; ENZYMES; GLUCOSE; GLYCEROL; NUTRITION; RATS; TISSUE;

INSULIN;

2 ARACHIDONOYLGLYCEROL; FATTY ACID; GLUCOSE; GLYCEROL; INSULIN; LARD;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; FAT INTAKE; GLUCONEOGENESIS; GLUCOSE TRANSPORT; HORMONAL REGULATION; HYPOTHALAMUS; IN VIVO STUDY; INSULIN RESISTANCE; LIPOLYSIS; MALE; MEDIOBASAL HYPOTHALAMUS; NONHUMAN; OVERNUTRITION; PRIORITY JOURNAL; RAT; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; DIABETES MELLITUS, TYPE 2; DIETARY FATS; ENERGY INTAKE; GLUCOSE; GLYCEROL; HUMANS; HYPOTHALAMUS; INSULIN; INSULIN RESISTANCE; LIPOLYSIS; MALE; OBESITY; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

RATTUS;

EID: 84866525104     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.307348     Document Type: Article

References (53)

1. Garg, A. (2004) Acquired and inherited lipodystrophies. N. Engl. J. Med. 350, 1220-1234
2. Mittendorfer, B., Magkos, F., Fabbrini, E., Mohammed, B. S., and Klein, S. (2009) Relationship between body fat mass and free fatty acid kinetics in men and women. Obesity 17, 1872-1877
3. Groop, L. C., Saloranta, C., Shank, M., Bonadonna, R. C., Ferrannini, E., and DeFronzo, R. A. (1991) The role of free fatty acid metabolism in the pathogenesis of insulin resistance in obesity and noninsulin-dependent diabetes mellitus. J. Clin. Endocrinol. Metab. 72, 96-107 (Pubitemid 21921662)
4. Roust, L. R., and Jensen, M. D. (1993) Postprandial free fatty acid kinetics are abnormal in upper body obesity. Diabetes 42, 1567-1573 (Pubitemid 23318111)
5. Groop, L. C., Bonadonna, R. C., DelPrato, S., Ratheiser, K., Zyck, K., Ferrannini, E., and DeFronzo, R. A. (1989) Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance. J. Clin. Invest. 84, 205-213 (Pubitemid 19170111)
6. Boden, G. (2006) Fatty acid-induced inflammation and insulin resistance in skeletal muscle and liver. Curr. Diab Rep. 6, 177-181
7. Boden, G., Chen, X., Ruiz, J., White, J. V., and Rossetti, L. (1994) Mechanisms of fatty acid-induced inhibition of glucose uptake. J. Clin. Invest. 93, 2438-2446 (Pubitemid 24177157)
8. Roden, M., Price, T. B., Perseghin, G., Petersen, K. F., Rothman, D. L., Cline, G. W., and Shulman, G. I. (1996) Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 97, 2859-2865 (Pubitemid 26197099)
9. Ferrannini, E., Barrett, E. J., Bevilacqua, S., and DeFronzo, R. A. (1983) Effect of fatty acids on glucose production and utilization in man. J. Clin. Invest. 72, 1737-1747 (Pubitemid 14229053)
10. Boden, G., Cheung, P., Stein, T. P., Kresge, K., and Mozzoli, M. (2002) FFA cause hepatic insulin resistance by inhibiting insulin suppression of glycogenolysis. Am. J. Physiol. Endocrinol. Metab. 283, E12-E19 (Pubitemid 34686662)
11. Degerman, E., Landström, T. R., Holst, L. S., Göransson, O., Härndahl, L., Ahmad, F., Choi, Y.-H., Masciarelli, S., Liu, H., and Manganiello, V. (2003) Role for phosphodiesterase 3B in regulation of lipolysis and insulin secretion, in Diabetes Mellitus: A Fundamental and Clinical Text (LeRoith, D., Olefsky, J. M., and Taylor, S. I., eds) 3rd Ed., pp. 374-381, Lippincott Williams & Wilkins, Philadelphia, PA
12. Assimacopoulos-Jeannet, F., Brichard, S., Rencurel, F., Cusin, I., and Jeanrenaud, B. (1995) In vivo effects of hyperinsulinemia on lipogenic enzymes and glucose transporter expression in rat liver and adipose tissues. Metabolism 44, 228-233
13. Scherer, T., O'Hare, J., Diggs-Andrews, K., Schweiger, M., Cheng, B., Lindtner, C., Zielinski, E., Vempati, P., Su, K., Dighe, S., Milsom, T., Puchowicz, M., Scheja, L., Zechner, R., Fisher, S. J., Previs, S. F., and Buettner, C. (2011) Brain insulin controls adipose tissue lipolysis and lipogenesis. Cell Metab. 13, 183-194
14. Rebrin, K., Steil, G. M., Mittelman, S. D., and Bergman, R. N. (1996) Causal linkage between insulin suppression of lipolysis and suppression of liver glucose output in dogs. J. Clin. Invest. 98, 741-749 (Pubitemid 26349179)
15. Rebrin, K., Steil, G. M., Getty, L., and Bergman, R. N. (1995) Free fatty acid as a link in the regulation of hepatic glucose output by peripheral insulin. Diabetes 44, 1038-1045
16. Wang, J., Obici, S., Morgan, K., Barzilai, N., Feng, Z., and Rossetti, L. (2001) Overfeeding rapidly induces leptin and insulin resistance. Diabetes 50, 2786-2791 (Pubitemid 33733130)
17. Kraegen, E. W., Clark, P. W., Jenkins, A. B., Daley, E. A., Chisholm, D. J., and Storlien, L. H. (1991) Development of muscle insulin resistance after liver insulin resistance in high-fat-fed rats. Diabetes 40, 1397-1403
18. Cornier, M. A., Bergman, B. C., and Bessesen, D. H. (2006) The effects of short-term overfeeding on insulin action in lean and reduced-obese individuals. Metabolism 55, 1207-1214 (Pubitemid 44215940)
19. Brøns, C., Jensen, C. B., Storgaard, H., Hiscock, N. J., White, A., Appel, J. S., Jacobsen, S., Nilsson, E., Larsen, C. M., Astrup, A., Quistorff, B., and Vaag, A. (2009) Impact of short-term high-fat feeding on glucose and insulin metabolism in young healthy men. J. Physiol. 587, 2387-2397
20. O'Hare, J. D., Zielinski, E., Cheng, B., Scherer, T., and Buettner, C. (2011) Central endocannabinoid signaling regulates hepatic glucose production and systemic lipolysis. Diabetes 60, 1055-1062
21. Wang, L., Liu, J., Harvey-White, J., Zimmer, A., and Kunos, G. (2003) Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc. Natl. Acad. Sci. U.S.A. 100, 1393-1398 (Pubitemid 36184012)
22. Obici, S., Zhang, B. B., Karkanias, G., and Rossetti, L. (2002) Hypothalamic insulin signaling is required for inhibition of glucose production. Nat. Med. 8, 1376-1382 (Pubitemid 36019422)
23. Pocai, A., Lam, T. K., Gutierrez-Juarez, R., Obici, S., Schwartz, G. J., Bryan, J., Aguilar-Bryan, L., and Rossetti, L. (2005) Hypothalamic K(ATP) channels control hepatic glucose production. Nature 434, 1026-1031 (Pubitemid 40586051)
24. Liu, L., Karkanias, G. B., Morales, J. C., Hawkins, M., Barzilai, N., Wang, J., and Rossetti, L. (1998) Intracerebroventricular leptin regulates hepatic but not peripheral glucose fluxes. J. Biol. Chem. 273, 31160-31167 (Pubitemid 28533128)
25. Kang, L., Chen, X., Sebastian, B. M., Pratt, B. T., Bederman, I. R., Alexander, J. C., Previs, S. F., and Nagy, L. E. (2007) Chronic ethanol and triglyceride turnover in white adipose tissue in rats. Inhibition of the anti-lipolytic action of insulin after chronic ethanol contributes to increased triglyceride degradation. J. Biol. Chem. 282, 28465-28473 (Pubitemid 47606032)
26. Buettner, C., Muse, E. D., Cheng, A., Chen, L., Scherer, T., Pocai, A., Su, K., Cheng, B., Li, X., Harvey-White, J., Schwartz, G. J., Kunos, G., and Rossetti, L. (2008) Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat. Med. 14, 667-675 (Pubitemid 351809549)
27. Buettner, C., Pocai, A., Muse, E. D., Etgen, A. M., Myers, M. G., Jr., and Rossetti, L. (2006) Critical role of STAT3 in leptin's metabolic actions. Cell Metab. 4, 49-60 (Pubitemid 43942253)
28. Ramnanan, C. J., Saraswathi, V., Smith, M. S., Donahue, E. P., Farmer, B., Farmer, T. D., Neal, D., Williams, P. E., Lautz, M., Mari, A., Cherrington, A. D., and Edgerton, D. S. (2011) Brain insulin action augments hepatic glycogen synthesis without suppressing glucose production or gluconeogenesis in dogs. J. Clin. Investig. 121, 3713-3723
29. Coomans, C. P., Geerling, J. J., Guigas, B., van den Hoek, A. M., Parlevliet, E. T., Ouwens, D. M., Pijl, H., Voshol, P. J., Rensen, P. C., Havekes, L. M., and Romijn, J. A. (2011) Circulating insulin stimulates fatty acid retention in white adipose tissue via KATP channel activation in the central nervous system only in insulin-sensitive mice. J. Lipid Res. 52, 1712-1722
30. McQuaid, S. E., Hodson, L., Neville, M. J., Dennis, A. L., Cheeseman, J., Humphreys, S. M., Ruge, T., Gilbert, M., Fielding, B. A., Frayn, K. N., and Karpe, F. (2011) Downregulation of adipose tissue fatty acid trafficking in obesity. A driver for ectopic fat deposition? Diabetes 60, 47-55
31. Könner, A. C., Janoschek, R., Plum, L., Jordan, S. D., Rother, E., Ma, X., Xu, C., Enriori, P., Hampel, B., Barsh, G. S., Kahn, C. R., Cowley, M. A., Ashcroft, F. M., and Brüning, J. C. (2007) Insulin action in AgRP-expressing neurons is required for suppression of hepatic glucose production. Cell Metab. 5, 438-449
32. Samuel, V. T., Liu, Z. X., Qu, X., Elder, B. D., Bilz, S., Befroy, D., Romanelli, A. J., and Shulman, G. I. (2004) Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J. Biol. Chem. 279, 32345-32353 (Pubitemid 39014687)
33. Pocai, A., Morgan, K., Buettner, C., Gutierrez-Juarez, R., Obici, S., and Rossetti, L. (2005) Central leptin acutely reverses diet-induced hepatic insulin resistance. Diabetes 54, 3182-3189 (Pubitemid 43334373)
34. Gutiérrez-Juárez, R., Obici, S., and Rossetti, L. (2004) Melanocortin-independent effects of leptin on hepatic glucose fluxes. J. Biol. Chem. 279, 49704-49715 (Pubitemid 39577774)
35. Lam, T. K., Pocai, A., Gutierrez-Juarez, R., Obici, S., Bryan, J., Aguilar-Bryan, L., Schwartz, G. J., and Rossetti, L. (2005) Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat. Med. 11, 320-327 (Pubitemid 40460561)
36. Di Marzo, V., Goparaju, S. K., Wang, L., Liu, J., Bátkai, S., Járai, Z., Fezza, F., Miura, G. I., Palmiter, R. D., Sugiura, T., and Kunos, G. (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410, 822-825 (Pubitemid 32303781)
37. Mølhøj, S., Hansen, H. S., Schweiger, M., Zimmermann, R., Johansen, T., and Malmlöf, K. (2010) Effect of the cannabinoid receptor-1 antagonist rimonabant on lipolysis in rats. Eur. J. Pharmacol. 646, 38-45
38. Hallschmid, M., Benedict, C., Schultes, B., Born, J., and Kern, W. (2008) Towards the therapeutic use of intranasal neuropeptide administration in metabolic and cognitive disorders. Int. J. Obes. (Lond.) 32, 275-282
39. Paolisso, G., Tataranni, P. A., Foley, J. E., Bogardus, C., Howard, B. V., and Ravussin, E. (1995) A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 38, 1213-1217
40. Bartness, T. J., Shrestha, Y. B., Vaughan, C. H., Schwartz, G. J., and Song, C. K. (2010) Sensory and sympathetic nervous system control of white adipose tissue lipolysis. Mol. Cell. Endocrinol. 318, 34-43
41. Li, J. H., Gautam, D., Han, S. J., Guettier, J. M., Cui, Y., Lu, H., Deng, C., O'Hare, J., Jou, W., Gavrilova, O., Buettner, C., and Wess, J. (2009) Hepatic muscarinic acetylcholine receptors are not critically involved in maintaining glucose homeostasis in mice. Diabetes 58, 2776-2787
42. Cote, M., Matias, I., Lemieux, I., Petrosino, S., Almeras, N., Despres, J. P., and Di Marzo, V. (2007) Circulating endocannabinoid levels, abdominal adiposity and related cardiometabolic risk factors in obese men. Int. J. Obes. (Lond.) 31, 692-699 (Pubitemid 46482358)
43. Blüher, M., Engeli, S., Klöting, N., Berndt, J., Fasshauer, M., Bátkai, S., Pacher, P., Schön, M. R., Jordan, J., and Stumvoll, M. (2006) Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity. Diabetes 55, 3053-3060 (Pubitemid 44923642)
44. Kim, W., Doyle, M. E., Liu, Z., Lao, Q., Shin, Y. K., Carlson, O. D., Kim, H. S., Thomas, S., Napora, J. K., Lee, E. K., Moaddel, R., Wang, Y., Maudsley, S., Martin, B., Kulkarni, R. N., and Egan, J. M. (2011) Cannabinoids inhibit insulin receptor signaling in pancreatic β-cells. Diabetes 60, 1198-1209
45. Nomura, D. K., Morrison, B. E., Blankman, J. L., Long, J. Z., Kinsey, S. G., Marcondes, M. C., Ward, A. M., Hahn, Y. K., Lichtman, A. H., Conti, B., and Cravatt, B. F. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334, 809-813
46. Zhang, X., Zhang, G., Zhang, H., Karin, M., Bai, H., and Cai, D. (2008) Hypothalamic IKKβ/NF-κB and ER stress link overnutrition to energy imbalance and obesity. Cell 135, 61-73
47. Thaler, J. P., Yi, C. X., Schur, E. A., Guyenet, S. J., Hwang, B. H., Dietrich, M. O., Zhao, X., Sarruf, D. A., Izgur, V., Maravilla, K. R., Nguyen, H. T., Fischer, J. D., Matsen, M. E., Wisse, B. E., Morton, G. J., Horvath, T. L., Baskin, D. G., Tschöp, M. H., and Schwartz, M. W. (2012) Obesity is associated with hypothalamic injury in rodents and humans. J. Clin. Investig. 122, 153-162
48. Tanimura, A., Yamazaki, M., Hashimotodani, Y., Uchigashima, M., Kawata, S., Abe, M., Kita, Y., Hashimoto, K., Shimizu, T., Watanabe, M., Sakimura, K., and Kano, M. (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase α mediates retrograde suppression of synaptic transmission. Neuron 65, 320-327
49. Dean, C. (2011) Endocannabinoid modulation of sympathetic and cardiovascular responses to acute stress in the periaqueductal gray of the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R771-R779
50. Niederhoffer, N., and Szabo, B. (2000) Cannabinoids cause central sympathoexcitation and bradycardia in rabbits. J. Pharmacol. Exp. Ther. 294, 707-713 (Pubitemid 30490848)
51. Brozoski, D. T., Dean, C., Hopp, F. A., Hillard, C. J., and Seagard, J. L. (2009) Differential endocannabinoid regulation of baroreflex-evoked sympathoinhibition in normotensive versus hypertensive rats. Auton. Neurosci. 150, 82-93
52. Morgan, K., Obici, S., and Rossetti, L. (2004) Hypothalamic responses to long-chain fatty acids are nutritionally regulated. J. Biol. Chem. 279, 31139-31148 (Pubitemid 39037776)
53. Lam, T. K. (2010) Neuronal regulation of homeostasis by nutrient sensing. Nat. Med. 16, 392-395