Cellular insulin resistance disrupts hypothalamic mHypoA-POMC/GFP neuronal signaling pathways

Journal of Endocrinology

Volumn 220, Issue 1, 2014, Pages 13-24

  Nazarians Armavil, Anaies ^a   Chalmers, Jennifer A ^a   Lee, Claire B ^a   Ye, Wenqing ^a   Belsham, Denise D ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Melanocortin synthesizing hormone; Cell biology; Hypothalamus; Insulin; Insulin resistance; Neuroendocrinology; Proopiomelanocortin

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; INSULIN; INSULIN RECEPTOR; MESSENGER RNA; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LINE; CONTROLLED STUDY; CYTOLOGY; ENZYME IMMUNOASSAY; HYPOTHALAMUS; IMMUNOFLUORESCENCE; INSULIN RESISTANCE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECOND MESSENGER; WESTERN BLOTTING;

Α-MELANOCORTIN-SYNTHESIZING HORMONE; CELL BIOLOGY; HYPOTHALAMUS; INSULIN; INSULIN RESISTANCE; NEUROENDOCRINOLOGY; PROOPIOMELANOCORTIN;

ALPHA-MSH; ANIMALS; BLOTTING, WESTERN; CELL LINE, TRANSFORMED; CILIARY NEUROTROPHIC FACTOR; DRUG RESISTANCE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HYPOGLYCEMIC AGENTS; HYPOTHALAMUS; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; PRO-OPIOMELANOCORTIN; PROMOTER REGIONS, GENETIC; RECEPTOR, INSULIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84890279800     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0334     Document Type: Article

References (47)

1. Air EL, Benoit SC, Clegg DJ, Seeley RJ & Woods SC 2002 Insulin and leptin combine additively to reduce food intake and body weight in rats. Endocrinology 143 2449-2452. (doi:10.1210/en.143.6.2449)
2. Ambati S, Duan J, DuffE, Choi YH, Hartzell DL, Della-Fera MA & Baile CA 2007 Gene expression in arcuate nucleus-median eminence of rats treated with leptin or ciliary neurotrophic factor. BioFactors 31 133-144. (doi:10.1002/biof.5520310204)
3. Arora S & Anubhuti 2006 Role of neuropeptides in appetite regulation and obesity - a review. Neuropeptides 40 375-401. (doi:10.1016/j.npep.2006. 07.001)
4. Baskin DG, Figlewicz Lattemann D, Seeley RJ, Woods SC, Porte D Jr & Schwartz MW 1999 Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Research 848 114-123. (doi:10.1016/S0006-8993(99)01974-5)
5. Belgardt BF, Husch A, Rother E, Ernst MB, Wunderlich FT, Hampel B, Klockener T, Alessi D, Kloppenburg P & Bruning JC 2008 PDK1 deficiency in POMC-expressing cells reveals FOXO1-dependent and -independent pathways in control of energy homeostasis and stress response. Cell Metabolism 7 291-301. (doi:10.1016/j.cmet.2008.01.006)
6. Belsham DD, Cai F, Cui H, Smukler SR, Salapatek AM & Shkreta L 2004 Generation of a phenotypic array of hypothalamic neuronal cell models to study complex neuroendocrine disorders. Endocrinology 145 393-400. (doi:10.1210/en.2003-0946)
7. Belsham DD, Fick LJ, Dalvi PS, Centeno ML, Chalmers JA, Lee PK, Wang Y, Drucker DJ & KoletarMM2009 Ciliary neurotrophic factor recruitment of glucagon-like peptide-1 mediates neurogenesis, allowing immortalization of adult murine hypothalamic neurons. FASEB Journal 23 4256-4265. (doi:10.1096/fj.09-133454)
8. Brown LM, Clegg DJ, Benoit SC & Woods SC 2006 Intraventricular insulin and leptin reduce food intake and body weight in C57BL/6J mice. Physiology & Behavior 89 687-691. (doi:10.1016/j.physbeh.2006.08. 008)
9. Chomczynski P & Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162 156-159. (doi:10.1016/0003-2697(87)90021-2)
10. Choudhury AI, Heffron H, Smith MA, Al-Qassab H, Xu AW, Selman C, Simmgen M, Clements M, Claret M, Maccoll G et al. 2005 The role of insulin receptor substrate 2 in hypothalamic and b cell function. Journal of Clinical Investigation 115 940-950. (doi:10.1172/JCI200524445)
11. Cone RD, Cowley MA, Butler AA, Fan W, Marks DL & Low MJ 2001 The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. International Journal of Obesity and Related Metabolic Disorders 25(Suppl 5) S63-S67. (doi:10.1038/sj.ijo.0801913)
12. Corkey BE 2012 Banting lecture 2011: hyperinsulinemia: cause or consequence? Diabetes 61 4-13. (doi:10.2337/db11-1483)
13. Couvreur O, Aubourg A, Crepin D, Degrouard J, Gertler A, Taouis M & Vacher CM 2011 The anorexigenic cytokine ciliary neurotrophic factor stimulates POMC gene expression via receptors localized in the nucleus of arcuate neurons. American Journal of Physiology. Endocrinology and Metabolism 302 E458-E467. (doi:10.1152/ajpendo.00388.2011)
14. Dhillon SS, McFadden SA, Chalmers JA, Centeno ML, KimGL&BelshamDD 2011 Cellular leptin resistance impairs the leptin-mediated suppression of neuropeptideYsecretion inhypothalamicneurons. Endocrinology 152 4138-4147. (doi:10.1210/en.2011-0178)
15. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR, Kuhar MJ, Saper CB & Elmquist JK 1998 Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21 1375-1385. (doi:10.1016/S0896-6273(00)80656-X)
16. HillJW, EliasCF, FukudaM, WilliamsKW, BerglundED, HollandWL, ChoYR, Chuang JC, Xu Y, Choi Met al. 2010 Direct insulin and leptin action on pro-opiomelanocortin neurons is required for normal glucose homeostasis and fertility. Cell Metabolism11 286-297. (doi:10.1016/j.cmet.2010. 03.002)
17. Iskandar K, CaoY, Hayashi Y, NakataM, TakanoE, YadaT, ZhangC, OgawaW, Oki M, Chua S Jr et al. 2010 PDK-1/FoxO1 pathway in POMC neurons regulates Pomc expression and food intake. American Journal of Physiology. Endocrinology and Metabolism 298 E787-E798. (doi:10.1152/ajpendo. 00512.2009)
18. Jamali AK & Tramu G 1997 Daily cycle of fos expression within hypothalamic POMC neurons of the male rat. Brain Research 771 45-54. (doi:10.1016/S0006-8993(97)00767-1)
19. Kaushik S, Arias E, Kwon H, Lopez NM, Athonvarangkul D, Sahu S, Schwartz GJ, Pessin JE & Singh R 2012 Loss of autophagy in hypothalamic POMC neurons impairs lipolysis. EMBO Reports 13 258-265. (doi:10.1038/embor.2011.260)
20. KimMS, Pak YK, Jang PG, Namkoong C, Choi YS, Won JC, Kim KS, Kim SW, Kim HS, Park JY et al. 2006 Role of hypothalamic Foxo1 in the regulation of food intake and energy homeostasis. Nature Neuroscience 9 901-906. (doi:10.1038/nn1731)
21. Kitamura T, Feng Y, Kitamura YI, Chua SC Jr, Xu AW, Barsh GS, Rossetti L & Accili D 2006 Forkhead protein FoxO1 mediates Agrp-dependent effects of leptin on food intake. Nature Medicine 12 534-540. (doi:10.1038/nm1392)
22. Kokoeva MV, Yin H & Flier JS 2005 Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310 679-683. (doi:10.1126/science.1115360)
23. Konner AC & Bruning JC 2012 Selective insulin and leptin resistance in metabolic disorders. Cell Metabolism 16 144-152. (doi:10.1016/j.cmet. 2012.07.004)
24. Lindberg I, van den Hurk WH, Bui C & Batie CJ 1995 Enzymatic characterization of immunopurified prohormone convertase 2: potent inhibition by a 7B2 peptide fragment. Biochemistry 34 5486-5493. (doi:10.1021/bi00016a020)
25. Mayer CM & Belsham DD 2010 Central insulin signaling is attenuated by long-term insulin exposure via insulin receptor substrate-1 serine phosphorylation, proteasomal degradation, and lysosomal insulin receptor degradation. Endocrinology 151 75-84. (doi:10.1210/en.2009-0838)
26. Mehran AE, TemplemanNM, BrigidiGS, LimGE, ChuKY, HuX, Botezelli JD, Asadi A, Hoffman BG, Kieffer TJ et al. 2013 Hyperinsulinemia drives dietinduced obesity independently of brain insulin production. Cell Metabolism 16 723-737. (doi:10.1016/j.cmet.2012.10.019)
27. Morton GJ, Cummings DE, Baskin DG, Barsh GS & Schwartz MW 2006 Central nervous system control of food intake and body weight. Nature 443 289-295. (doi:10.1038/nature05026)
28. Mountjoy KG 2010 Functions for pro-opiomelanocortin-derived peptides in obesity and diabetes. Biochemical Journal 428 305-324. (doi:10.1042/BJ20091957)
29. Mountjoy KG & Wong J 1997 Obesity, diabetes and functions for proopiomelanocortin-derived peptides. Molecular and Cellular Endocrinology 128 171-177. (doi:10.1016/S0303-7207(96)04017-8)
30. Nazarians-Armavil A, Menchella JA & Belsham DD 2013 Cellular insulin resistance disrupts leptin-mediated control of neuronal signaling and transcription. Molecular Endocrinology 27 990-1003. (doi:10.1210/me. 2012-1338)
31. Niswender KD, Morrison CD, Clegg DJ, Olson R, Baskin DG, Myers MG Jr, Seeley RJ & Schwartz MW 2003 Insulin activation of phosphatidylinositol 3-kinase in the hypothalamic arcuate nucleus: a key mediator of insulin-induced anorexia. Diabetes 52 227-231. (doi:10.2337/diabetes.52.2.227)
32. Padilla SL, Reef D & Zeltser LM 2012 Defining POMC neurons using transgenic reagents: impact of transient Pomc expression in diverse immature neuronal populations. Endocrinology 153 1219-1231. (doi:10.1210/en.2011-1665)
33. Parton LE, Ye CP, Coppari R, Enriori PJ, Choi B, Zhang CY, Xu C, Vianna CR, Balthasar N, Lee CE et al. 2007 Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449 228-232. (doi:10.1038/nature06098)
34. Plum L, Belgardt BF & Bruning JC 2006a Central insulin action in energy and glucose homeostasis. Journal of Clinical Investigation 116 1761-1766. (doi:10.1172/JCI29063)
35. Plum L, Ma X, Hampel B, Balthasar N, Coppari R, Munzberg H, Shanabrough M, Burdakov D, Rother E, Janoschek R et al. 2006b Enhanced PIP3 signaling in POMC neurons causes KATP channel activation and leads to diet-sensitive obesity. Journal of Clinical Investigation 116 1886-1901. (doi:10.1172/JCI27123)
36. Pritchard LE, Turnbull AV & White A 2002 Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signalling and obesity. Journal of Endocrinology 172 411-421. (doi:10.1677/joe.0. 1720411)
37. Purser MJ, Dalvi PS, Wang ZC & Belsham DD 2013 The cytokine ciliary neurotrophic factor (CNTF) activates hypothalamic urocortinexpressing neurons both in vitro and in vivo. PLoS ONE 8 e61616. (doi:10.1371/journal.pone.0061616)
38. Reusch JE, Bhuripanyo P, Carel K, Leitner JW, Hsieh P, DePaolo D & Draznin B 1995 Differential requirement for p21ras activation in the metabolic signaling by insulin. Journal of Biological Chemistry 270 2036-2040. (doi:10.1074/jbc.270.5.2036)
39. Sagar SM, Sharp FR & Curran T 1988 Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240 1328-1331. (doi:10.1126/science.3131879)
40. Thaler JP, Yi CX, Schur EA, Guyenet SJ, Hwang BH, Dietrich MO, Zhao X, Sarruf DA, Izgur V, Maravilla KR et al. 2012 Obesity is associated with hypothalamic injury in rodents and humans. Journal of Clinical Investigation 122 153-162. (doi:10.1172/JCI59660)
41. Varela L & Horvath TL 2012 Leptin and insulin pathways in POMC and AgRP neurons that modulate energy balance and glucose homeostasis. EMBO Reports 13 1079-1086. (doi:10.1038/embor.2012.174)
42. Vogt MC & Bruning JC 2013 CNS insulin signaling in the control of energy homeostasis and glucose metabolism - from embryo to old age. Trends in Endocrinology and Metabolism 24 76-84. (doi:10.1016/j.tem. 2012.11.004)
43. Williams KW, Margatho LO, Lee CE, Choi M, Lee S, Scott MM, Elias CF & Elmquist JK 2010 Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. Journal of Neuroscience 30 2472-2479. (doi:10.1523/JNEUROSCI.3118-09.2010)
44. Wittmann G, Hrabovszky E & Lechan RM 2013 Distinct glutamatergic and GABAergic subsets of hypothalamic proopiomelanocortin neurons revealed by in situ hybridization inmale rats and mice. Journal of Comparative Neurology 521 3287-3302. (doi:10.1002/cne.23350)
45. Xu Y, Jones JE, Kohno D, Williams KW, Lee CE, Choi MJ, Anderson JG, Heisler LK, Zigman JM, Lowell BB et al. 2008 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 60 582-589. (doi:10.1016/j.neuron.2008.09.033)
46. Xu Y, Berglund ED, Sohn JW, Holland WL, Chuang JC, Fukuda M, Rossi J, Williams KW, Jones JE, Zigman JM et al. 2010 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate insulin sensitivity in liver. Nature Neuroscience 13 1457-1459. (doi:10.1038/nn.2664)
47. Zhang X, Zhang G, Zhang H, Karin M, Bai H & Cai D 2008 Hypothalamic IKKβ/NF-κB and ER stress link overnutrition to energy imbalance and obesity. Cell 135 61-73. (doi:10.1016/j.cell.2008.07.043)