Activation of muscular TrkB by its small molecular agonist 7,8-dihydroxyflavone sex-dependently regulates energy metabolism in diet-induced obese mice

Chemistry and Biology

Volumn 22, Issue 3, 2015, Pages 355-368

  Chan, Chi Bun ^a,b   Tse, Margaret Chui Ling ^a,b   Liu, Xia ^a   Zhang, Shuai ^a   Schmidt, Robin ^a   Otten, Reed ^a   Liu, Liegang ^c   Ye, Keqiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

7,8 DIHYDROXYFLAVONE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INSULIN; UNCOUPLING PROTEIN 1; 6,7-DIHYDROXYFLAVONE; FLAVONE DERIVATIVE; MEMBRANE PROTEIN; NTRK2 PROTEIN, MOUSE; PROTEIN TYROSINE KINASE; TROPOMYOSIN-RELATED KINASE-B, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; ENERGY EXPENDITURE; ENERGY METABOLISM; ENZYME ACTIVITY; FEMALE; GASTROCNEMIUS MUSCLE; GENDER; GENE EXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INSULIN SENSITIVITY; KNOCKOUT MOUSE; LIPID DIET; LIPID OXIDATION; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; VASTUS LATERALIS MUSCLE; WEIGHT GAIN; 3T3 CELL LINE; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; HEK293 CELL LINE; MALE; METABOLISM; MOUSE MUTANT; OBESITY; TRANSGENIC MOUSE;

3T3-L1 CELLS; ANIMALS; DIET, HIGH-FAT; ENZYME ACTIVATION; FEMALE; FLAVONES; HEK293 CELLS; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; MICE, TRANSGENIC; OBESITY; PROTEIN-TYROSINE KINASES;

EID: 84924980688     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.02.003     Document Type: Article

References (54)

1. R. Andero, N. Daviu, R.M. Escorihuela, R. Nadal, and A. Armario 7,8-Dihydroxyflavone, a TrkB receptor agonist, blocks long-term spatial memory impairment caused by immobilization stress in rats Hippocampus 22 2012 399 408
2. H. Aquila, T.A. Link, and M. Klingenberg The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane EMBO J. 4 1985 2369 2376
3. J.E. Ayala, D.P. Bracy, O.P. McGuinness, and D.H. Wasserman Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse Diabetes 55 2006 390 397
4. Y. Bai, and G. Attardi The mtDNA-encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme EMBO J. 17 1998 4848 4858
5. D. Baker-Andresen, C.R. Flavell, X. Li, and T.W. Bredy Activation of BDNF signaling prevents the return of fear in female mice Learn. Mem. 20 2013 237 240
6. S. Burattini, P. Ferri, M. Battistelli, R. Curci, F. Luchetti, and E. Falcieri C2C12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization Eur. J. Histochem. 48 2004 223 233
7. C. Camerino, M. Zayzafoon, M. Rymaszewski, J. Heiny, M. Rios, and P.V. Hauschka Central depletion of brain-derived neurotrophic factor in mice results in high bone mass and metabolic phenotype Endocrinology 153 2012 5394 5405
8. B. Cannon, and J. Nedergaard Brown adipose tissue: function and physiological significance Physiol. Rev. 84 2004 277 359
9. C.B. Chan, X. Liu, D.Y. Jung, J.Y. Jun, H.R. Luo, J.K. Kim, and K. Ye Deficiency of phosphoinositide 3-kinase enhancer protects mice from diet-induced obesity and insulin resistance Diabetes 59 2010 883 893
10. D.E. Cummings, E.P. Brandon, J.V. Planas, K. Motamed, R.L. Idzerda, and G.S. McKnight Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A Nature 382 1996 622 626
11. R. Cuppini, S. Sartini, D. Agostini, M. Guescini, P. Ambrogini, M. Betti, L. Bertini, M. Vallasciani, and V. Stocchi Bdnf expression in rat skeletal muscle after acute or repeated exercise Arch. Ital. Biol. 145 2007 99 110
12. M. del Mar Gonzalez-Barroso, C. Pecqueur, C. Gelly, D. Sanchis, M.C. Alves-Guerra, F. Bouillaud, D. Ricquier, and A.M. Cassard-Doulcier Transcriptional activation of the human ucp1 gene in a rodent cell line. Synergism of retinoids, isoproterenol, and thiazolidinedione is mediated by a multipartite response element J. Biol. Chem. 275 2000 31722 31732
13. A.W. English, K. Liu, J.M. Nicolini, A.M. Mulligan, and K. Ye Small-molecule trkB agonists promote axon regeneration in cut peripheral nerves Proc. Natl. Acad. Sci. USA 110 2013 16217 16222
14. S. Finkbeiner, S.F. Tavazoie, A. Maloratsky, K.M. Jacobs, K.M. Harris, and M.E. Greenberg CREB: a major mediator of neuronal neurotrophin responses Neuron 19 1997 1031 1047
15. Z. Fu, W. Zhang, W. Zhen, H. Lum, J. Nadler, J. Bassaganya-Riera, Z. Jia, Y. Wang, H. Misra, and D. Liu Genistein induces pancreatic beta-cell proliferation through activation of multiple signaling pathways and prevents insulin-deficient diabetes in mice Endocrinology 151 2010 3026 3037
16. H. Funakoshi, J. Frisen, G. Barbany, T. Timmusk, O. Zachrisson, V.M. Verge, and H. Persson Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve J. Cell Biol. 123 1993 455 465
17. J. Gray, G.S. Yeo, J.J. Cox, J. Morton, A.L. Adlam, J.M. Keogh, J.A. Yanovski, A. El Gharbawy, J.C. Han, and Y.C. Tung et al. Hyperphagia, severe obesity, impaired cognitive function, and hyperactivity associated with functional loss of one copy of the brain-derived neurotrophic factor (BDNF) gene Diabetes 55 2006 3366 3371
18. V.K. Gupta, Y. You, J.C. Li, A. Klistorner, and S.L. Graham Protective effects of 7,8-dihydroxyflavone on retinal ganglion and RGC-5 cells against excitotoxic and oxidative stress J. Mol. Neurosci. 49 2013 96 104
19. D.H. Han, L.A. Nolte, J.S. Ju, T. Coleman, J.O. Holloszy, and C.F. Semenkovich UCP-mediated energy depletion in skeletal muscle increases glucose transport despite lipid accumulation and mitochondrial dysfunction Am. J. Physiol. Endocrinol. Metab. 286 2004 E347 353
20. D.G. Hardie, I.P. Salt, and S.P. Davies Analysis of the role of the AMP-activated protein kinase in the response to cellular stress Methods Mol. Biol. 99 2000 63 74
21. E.J. Huang, and L.F. Reichardt Neurotrophins: roles in neuronal development and function Annu. Rev. Neurosci. 24 2001 677 736
22. S.W. Jang, X. Liu, M. Yepes, K.R. Shepherd, G.W. Miller, Y. Liu, W.D. Wilson, G. Xiao, B. Blanchi, Y.E. Sun, and K. Ye A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone Proc. Natl. Acad. Sci. USA 107 2010 2687 2692
23. M. Jiang, Q. Peng, X. Liu, J. Jin, Z. Hou, J. Zhang, S. Mori, C.A. Ross, K. Ye, and W. Duan Small-molecule TrkB receptor agonists improve motor function and extend survival in a mouse model of Huntington's disease Hum. Mol. Genet. 22 2013 2462 2470
24. R.A. Johnson, M. Lam, A.M. Punzo, H. Li, B.R. Lin, K. Ye, G.S. Mitchell, and Q. Chang 7,8-dihydroxyflavone exhibits therapeutic efficacy in a mouse model of Rett syndrome J. Appl. Phys. (1985) 112 2012 704 710
25. S. Keipert, M. Ost, A. Chadt, A. Voigt, V. Ayala, M. Portero-Otin, R. Pamplona, H. Al-Hasani, and S. Klaus Skeletal muscle uncoupling-induced longevity in mice is linked to increased substrate metabolism and induction of the endogenous antioxidant defense system Am. J. Physiol. Endocrinol. Metab. 304 2013 E495 E506
26. S.G. Kernie, D.J. Liebl, and L.F. Parada BDNF regulates eating behavior and locomotor activity in mice EMBO J. 19 2000 1290 1300
27. S. Klaus, B. Rudolph, C. Dohrmann, and R. Wehr Expression of uncoupling protein 1 in skeletal muscle decreases muscle energy efficiency and affects thermoregulation and substrate oxidation Physiol. Genomics 21 2005 193 200
28. B. Li, L.A. Nolte, J.S. Ju, D.H. Han, T. Coleman, J.O. Holloszy, and C.F. Semenkovich Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice Nat. Med. 6 2000 1115 1120
29. X. Liu, C.B. Chan, S.W. Jang, S. Pradoldej, J. Huang, K. He, L.H. Phun, S. France, G. Xiao, and Y. Jia et al. A synthetic 7,8-dihydroxyflavone derivative promotes neurogenesis and exhibits potent antidepressant effect J. Med. Chem. 53 2010 8274 8286
30. X. Liu, Q. Qi, G. Xiao, J. Li, H.R. Luo, and K. Ye O-methylated metabolite of 7,8-dihydroxyflavone activates TrkB receptor and displays antidepressant activity Pharmacology 91 2013 185 200
31. T. Matsuzaka, H. Shimano, N. Yahagi, T. Kato, A. Atsumi, T. Yamamoto, N. Inoue, M. Ishikawa, S. Okada, and N. Ishigaki et al. Crucial role of a long-chain fatty acid elongase, Elovl6, in obesity-induced insulin resistance Nat. Med. 13 2007 1193 1202
32. V.B. Matthews, M.B. Astrom, M.H. Chan, C.R. Bruce, K.S. Krabbe, O. Prelovsek, T. Akerstrom, C. Yfanti, C. Broholm, and O.H. Mortensen et al. Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase Diabetologia 52 2009 1409 1418
33. L.M. Monteggia, B. Luikart, M. Barrot, D. Theobold, I. Malkovska, S. Nef, L.F. Parada, and E.J. Nestler Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors Biol. Psychiatry 61 2007 187 197
34. T. Nakagawa, A. Tsuchida, Y. Itakura, T. Nonomura, M. Ono, F. Hirota, T. Inoue, C. Nakayama, M. Taiji, and H. Noguchi Brain-derived neurotrophic factor regulates glucose metabolism by modulating energy balance in diabetic mice Diabetes 49 2000 436 444
35. S. Neschen, Y. Katterle, J. Richter, R. Augustin, S. Scherneck, F. Mirhashemi, A. Schurmann, H.G. Joost, and S. Klaus Uncoupling protein 1 expression in murine skeletal muscle increases AMPK activation, glucose turnover, and insulin sensitivity in vivo Physiol. Genomics 33 2008 333 340
36. T. Numakawa, S. Suzuki, E. Kumamaru, N. Adachi, M. Richards, and H. Kunugi BDNF function and intracellular signaling in neurons Histol. Histopathol. 25 2010 237 258
37. M.A. Pelleymounter, M.J. Cullen, and C.L. Wellman Characteristics of BDNF-induced weight loss Exp. Neurol. 131 1995 229 238
38. J.F. Poduslo, and G.L. Curran Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF Brain Res. Mol. Brain Res. 36 1996 280 286
39. M. Reich, T. Liefeld, J. Gould, J. Lerner, P. Tamayo, and J.P. Mesirov GenePattern 2.0 Nat. Genet. 38 2006 500 501
40. J.S. Rim, and L.P. Kozak Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene J. Biol. Chem. 277 2002 34589 34600
41. M. Rios BDNF and the central control of feeding: accidental bystander or essential player? Trends Neurosci. 36 2013 83 90
42. D.L. Shelton, J. Sutherland, J. Gripp, T. Camerato, M.P. Armanini, H.S. Phillips, K. Carroll, S.D. Spencer, and A.D. Levinson Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins J. Neurosci. 15 1995 477 491
43. J.L. Spencer, E.M. Waters, T.A. Milner, and B.S. McEwen Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice Neuroscience 155 2008 1106 1119
44. C. Sztalryd, G. Xu, H. Dorward, J.T. Tansey, J.A. Contreras, A.R. Kimmel, and C. Londos Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation J. Cell Biol. 161 2003 1093 1103
45. P. Tapley, F. Lamballe, and M. Barbacid K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors Oncogene 7 1992 371 381
46. Y.H. Tseng, E. Kokkotou, T.J. Schulz, T.L. Huang, J.N. Winnay, C.M. Taniguchi, T.T. Tran, R. Suzuki, D.O. Espinoza, and Y. Yamamoto et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure Nature 454 2008 1000 1004
47. A. Tsuchida, T. Nonomura, M. Ono-Kishino, T. Nakagawa, M. Taiji, and H. Noguchi Acute effects of brain-derived neurotrophic factor on energy expenditure in obese diabetic mice Int. J. Obes. Relat. Metab. Disord. 25 2001 1286 1293
48. K. Uluc, P. Kendigelen, E. Fidan, L. Zhang, V. Chanana, D. Kintner, E. Akture, C. Song, K. Ye, and D. Sun et al. TrkB receptor agonist 7, 8 dihydroxyflavone triggers profound gender-dependent neuroprotection in mice after perinatal hypoxia and ischemia CNS Neurol. Disord. Drug Targets 12 2013 360 370
49. T.J. Unger, G.A. Calderon, L.C. Bradley, M. Sena-Esteves, and M. Rios Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity J. Neurosci. 27 2007 14265 14274
50. C. Wang, E. Bomberg, C.J. Billington, A.S. Levine, and C.M. Kotz Brain-derived neurotrophic factor (BDNF) in the hypothalamic ventromedial nucleus increases energy expenditure Brain Res. 1336 2010 66 77
51. G.S. Yeo, C.C. Connie Hung, J. Rochford, J. Keogh, J. Gray, S. Sivaramakrishnan, S. O'Rahilly, and I.S. Farooqi A de novo mutation affecting human TrkB associated with severe obesity and developmental delay Nat. Neurosci. 7 2004 1187 1189
52. Q. Yu, Q. Chang, X. Liu, Y. Wang, H. Li, S. Gong, K. Ye, and X. Lin Protection of spiral ganglion neurons from degeneration using small-molecule TrkB receptor agonists J. Neurosci. 33 2013 13042 13052
53. Z. Zhang, X. Liu, J.P. Schroeder, C.B. Chan, M. Song, S.P. Yu, D. Weinshenker, and K. Ye 7,8-Dihydroxyflavone prevents synaptic loss and memory deficits in a mouse model of Alzheimer's disease Neuropsychopharmacology 39 2013 638 650
54. Y. Zhou, L. Jiang, and L. Rui Identification of MUP1 as a regulator for glucose and lipid metabolism in mice J. Biol. Chem. 284 2009 11152 11159