The thermogenic effect of leptin is dependent on a distinct population of prolactin-releasing peptide neurons in the dorsomedial hypothalamus

Cell Metabolism

Volumn 20, Issue 4, 2014, Pages 639-649

  Dodd, Garron T ^a   Worth, Amy A ^a   Nunn, Nicolas ^a   Korpal, Aaron K ^a   Bechtold, David A ^a   Allison, Margaret B ^b   Myers, Martin G ^b   Statnick, Michael A ^c   Luckman, Simon M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ; CRE RECOMBINASE; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA; PROLACTIN RELEASING FACTOR; RFAMIDE PROLACTIN RELEASING PEPTIDE; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CALORIC INTAKE; CELL POPULATION; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; ENERGY EXPENDITURE; ENZYME REACTIVATION; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NERVE CELL; NONHUMAN; OBESITY; PHENOTYPE; PROTEIN EXPRESSION; STOP CODON; THERMOGENESIS; ALLELE; ANIMAL; DEFICIENCY; ENERGY METABOLISM; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ALLELES; ANIMALS; CHOLECYSTOKININ; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; ENERGY METABOLISM; LEPTIN; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; OBESITY; PROLACTIN-RELEASING HORMONE; RECEPTORS, LEPTIN; THERMOGENESIS;

EID: 84907968471     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.07.022     Document Type: Article

References (51)

1. A. Alingh Prins, A. de Jong-Nagelsmit, J. Keijser, and J.H. Strubbe Daily rhythms of feeding in the genetically obese and lean Zucker rats Physiol. Behav. 38 1986 423 426
2. N. Balthasar, R. Coppari, J. McMinn, S.M. Liu, C.E. Lee, V. Tang, C.D. Kenny, R.A. McGovern, S.C. Chua Jr., J.K. Elmquist, and B.B. Lowell Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis Neuron 42 2004 983 991
3. N. Balthasar, L.T. Dalgaard, C.E. Lee, J. Yu, H. Funahashi, T. Williams, M. Ferreira, V. Tang, R.A. McGovern, and C.D. Kenny Divergence of melanocortin pathways in the control of food intake and energy expenditure Cell 123 2005 493 505
4. D.A. Bechtold, and S.M. Luckman Prolactin-releasing Peptide mediates cholecystokinin-induced satiety in mice Endocrinology 147 2006 4723 4729
5. D.A. Bechtold, and S.M. Luckman The role of RFamide peptides in feeding J. Endocrinol. 192 2007 3 15
6. S. Bi, E.E. Ladenheim, G.J. Schwartz, and T.H. Moran A role for NPY overexpression in the dorsomedial hypothalamus in hyperphagia and obesity of OLETF rats Am. J. Physiol. Regul. Integr. Comp. Physiol. 281 2001 R254 R260
7. S. Bi, B.M. Robinson, and T.H. Moran Acute food deprivation and chronic food restriction differentially affect hypothalamic NPY mRNA expression Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 2003 R1030 R1036
8. B. Cannon, and J. Nedergaard Brown adipose tissue: function and physiological significance Physiol. Rev. 84 2004 277 359
9. P.T. Chao, L. Yang, S. Aja, T.H. Moran, and S. Bi Knockdown of NPY expression in the dorsomedial hypothalamus promotes development of brown adipocytes and prevents diet-induced obesity Cell Metab. 13 2011 573 583
10. C. Chen, S.L. Dun, N.J. Dun, and J.K. Chang Prolactin-releasing peptide-immunoreactivity in A1 and A2 noradrenergic neurons of the rat medulla Brain Res. 822 1999 276 279
11. C. de Luca, T.J. Kowalski, Y. Zhang, J.K. Elmquist, C. Lee, M.W. Kilimann, T. Ludwig, S.M. Liu, and S.C. Chua Jr. Complete rescue of obesity, diabetes, and infertility in db/db mice by neuron-specific LEPR-B transgenes J. Clin. Invest. 115 2005 3484 3493
12. H. Dhillon, J.M. Zigman, C. Ye, C.E. Lee, R.A. McGovern, V. Tang, C.D. Kenny, L.M. Christiansen, R.D. White, and E.A. Edelstein Leptin directly activates SF1 neurons in the VMH, and this action by leptin is required for normal body-weight homeostasis Neuron 49 2006 191 203
13. G.T. Dodd, and S.M. Luckman Physiological Roles of GPR10 and PrRP Signaling Front. Endocrinol. (Lausanne) 4 2013 10.3389/fendo.2013.00020
14. G.T. Dodd, A.A. Worth, D.J. Hodkinson, R.K. Srivastava, B. Lutz, S.R. Williams, and S.M. Luckman Central functional response to the novel peptide cannabinoid, hemopressin Neuropharmacology 71 2013 27 36
15. S. Draper, M. Kirigiti, M. Glavas, B. Grayson, C.N. Chong, B. Jiang, M.S. Smith, L.M. Zeltser, and K.L. Grove Differential gene expression between neuropeptide Y expressing neurons of the dorsomedial nucleus of the hypothalamus and the arcuate nucleus: microarray analysis study Brain Res. 1350 2010 139 150
16. K.L. Ellacott, C.B. Lawrence, N.J. Rothwell, and S.M. Luckman PRL-releasing peptide interacts with leptin to reduce food intake and body weight Endocrinology 143 2002 368 374
17. P.J. Enriori, P. Sinnayah, S.E. Simonds, C. Garcia Rudaz, and M.A. Cowley Leptin action in the dorsomedial hypothalamus increases sympathetic tone to brown adipose tissue in spite of systemic leptin resistance J. Neurosci. 31 2011 12189 12197
18. M.B. Ernst, C.M. Wunderlich, S. Hess, M. Paehler, A. Mesaros, S.B. Koralov, A. Kleinridders, A. Husch, H. Münzberg, and B. Hampel Enhanced Stat3 activation in POMC neurons provokes negative feedback inhibition of leptin and insulin signaling in obesity J. Neurosci. 29 2009 11582 11593
19. A. Funakoshi, K. Miyasaka, H. Shinozaki, M. Masuda, T. Kawanami, Y. Takata, and A. Kono An animal model of congenital defect of gene expression of cholecystokinin (CCK)-A receptor Biochem. Biophys. Res. Commun. 210 1995 787 796
20. W. Gu, B.J. Geddes, C. Zhang, K.P. Foley, and A. Stricker-Krongrad The prolactin-releasing peptide receptor (GPR10) regulates body weight homeostasis in mice J. Mol. Neurosci. 22 2004 93 103
21. Z. Hawke, T.R. Ivanov, D.A. Bechtold, H. Dhillon, B.B. Lowell, and S.M. Luckman PACAP neurons in the hypothalamic ventromedial nucleus are targets of central leptin signaling J. Neurosci. 29 2009 14828 14835
22. W.G. Haynes, D.A. Morgan, A. Djalali, W.I. Sivitz, and A.L. Mark Interactions between the melanocortin system and leptin in control of sympathetic nerve traffic Hypertension 33 1999 542 547
23. S. Hinuma, Y. Habata, R. Fujii, Y. Kawamata, M. Hosoya, S. Fukusumi, C. Kitada, Y. Masuo, T. Asano, and H. Matsumoto A prolactin-releasing peptide in the brain Nature 393 1998 272 276
24. K.P. Hummel, M.M. Dickie, and D.L. Coleman Diabetes, a new mutation in the mouse Science 153 1966 1127 1128
25. Z. Jovanovic, Y.C. Tung, B.Y. Lam, S. O'Rahilly, and G.S. Yeo Identification of the global transcriptomic response of the hypothalamic arcuate nucleus to fasting and leptin J. Neuroendocrinol. 22 2010 915 925
26. K.W. Kim, L. Zhao, J. Donato Jr., D. Kohno, Y. Xu, C.F. Elias, C. Lee, K.L. Parker, and J.K. Elmquist Steroidogenic factor 1 directs programs regulating diet-induced thermogenesis and leptin action in the ventral medial hypothalamic nucleus Proc. Natl. Acad. Sci. USA 108 2011 10673 10678
27. D. Kong, Q. Tong, C. Ye, S. Koda, P.M. Fuller, M.J. Krashes, L. Vong, R.S. Ray, D.P. Olson, and B.B. Lowell GABAergic RIP-Cre neurons in the arcuate nucleus selectively regulate energy expenditure Cell 151 2012 645 657
28. C.B. Lawrence, F. Celsi, J. Brennand, and S.M. Luckman Alternative role for prolactin-releasing peptide in the regulation of food intake Nat. Neurosci. 3 2000 645 646
29. C.B. Lawrence, K.L. Ellacott, and S.M. Luckman PRL-releasing peptide reduces food intake and may mediate satiety signaling Endocrinology 143 2002 360 367
30. C.B. Lawrence, Y.L. Liu, M.J. Stock, and S.M. Luckman Anorectic actions of prolactin-releasing peptide are mediated by corticotropin-releasing hormone receptors Am. J. Physiol. Regul. Integr. Comp. Physiol. 286 2004 R101 R107
31. S.J. Lee, M. Kirigiti, S.R. Lindsley, A. Loche, C.J. Madden, S.F. Morrison, M.S. Smith, and K.L. Grove Efferent projections of neuropeptide Y-expressing neurons of the dorsomedial hypothalamus in chronic hyperphagic models J. Comp. Neurol. 521 2013 1891 1914
32. R.L. Leshan, G.W. Louis, Y.H. Jo, C.J. Rhodes, H. Münzberg, and M.G. Myers Jr. Direct innervation of GnRH neurons by metabolic- and sexual odorant-sensing leptin receptor neurons in the hypothalamic ventral premammillary nucleus J. Neurosci. 29 2009 3138 3147
33. K. Loh, A. Fukushima, X. Zhang, S. Galic, D. Briggs, P.J. Enriori, S. Simonds, F. Wiede, A. Reichenbach, and C. Hauser Elevated hypothalamic TCPTP in obesity contributes to cellular leptin resistance Cell Metab. 14 2011 684 699
34. C.L. McLaughlin, and C.A. Baile Ontogeny of feeding behavior in the Zucker obese rat Physiol. Behav. 26 1981 607 612
35. J.E. McMinn, D.K. Sindelar, P.J. Havel, and M.W. Schwartz Leptin deficiency induced by fasting impairs the satiety response to cholecystokinin Endocrinology 141 2000 4442 4448
36. J.E. McMinn, S.M. Liu, I. Dragatsis, P. Dietrich, T. Ludwig, S. Eiden, and S.C. Chua Jr. An allelic series for the leptin receptor gene generated by CRE and FLP recombinase Mamm. Genome 15 2004 677 685
37. J.G. Mercer, N. Hoggard, L.M. Williams, C.B. Lawrence, L.T. Hannah, and P. Trayhurn Localization of leptin receptor mRNA and the long form splice variant (Ob-Rb) in mouse hypothalamus and adjacent brain regions by in situ hybridization FEBS Lett. 387 1996 113 116
38. S.F. Morrison, K. Nakamura, and C.J. Madden Central control of thermogenesis in mammals Exp. Physiol. 93 2008 773 797
39. H. Münzberg, L. Huo, E.A. Nillni, A.N. Hollenberg, and C. Bjørbaek Role of signal transducer and activator of transcription 3 in regulation of hypothalamic proopiomelanocortin gene expression by leptin Endocrinology 144 2003 2121 2131
40. M.G. Myers Jr., H. Münzberg, G.M. Leinninger, and R.L. Leshan The geometry of leptin action in the brain: more complicated than a simple ARC Cell Metab. 9 2009 117 123
41. G. Paxinos, and K.B.J. Franklin The mouse brain 2001 Academic Press San Diego, CA
42. W.K. Samson, Z.T. Resch, T.C. Murphy, and J.K. Chang Gender-biased activity of the novel prolactin releasing peptides: comparison with thyrotropin releasing hormone reveals only pharmacologic effects Endocrine 9 1998 289 291
43. P.J. Scarpace, and M. Matheny Leptin induction of UCP1 gene expression is dependent on sympathetic innervation Am. J. Physiol. 275 1998 E259 E264
44. Y.C. Shi, J. Lau, Z. Lin, H. Zhang, L. Zhai, G. Sperk, R. Heilbronn, M. Mietzsch, S. Weger, and X.F. Huang Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN Cell Metab. 17 2013 236 248
45. Y. Takayanagi, H. Matsumoto, M. Nakata, T. Mera, S. Fukusumi, S. Hinuma, Y. Ueta, T. Yada, G. Leng, and T. Onaka Endogenous prolactin-releasing peptide regulates food intake in rodents J. Clin. Invest. 118 2008 4014 4024
46. P. Trayhurn Thermoregulation in the diabetic-obese (db/db) mouse. The role of non-shivering thermogenesis in energy balance Pflugers Arch. 380 1979 227 232
47. P. Trayhurn, P.L. Thurlby, and W.P. James Thermogenic defect in pre-obese ob/ob mice Nature 266 1977 60 62
48. E. van de Wall, R. Leshan, A.W. Xu, N. Balthasar, R. Coppari, S.M. Liu, Y.H. Jo, R.G. Mackenzie, D.B. Allison, and N.J. Dun Collective and individual functions of leptin receptor modulated neurons controlling metabolism and ingestion Endocrinology 149 2007 1773 1785
49. T.K. Watanabe, M. Suzuki, Y. Yamasaki, S. Okuno, H. Hishigaki, T. Ono, K. Oga, A. Mizoguchi-Miyakita, A. Tsuji, and N. Kanemoto Mutated G-protein-coupled receptor GPR10 is responsible for the hyperphagia/dyslipidaemia/obesity locus of Dmo1 in the OLETF rat Clin. Exp. Pharmacol. Physiol. 32 2005 355 366
50. L. Yang, K.A. Scott, J. Hyun, K.L. Tamashiro, N. Tray, T.H. Moran, and S. Bi Role of dorsomedial hypothalamic neuropeptide Y in modulating food intake and energy balance J. Neurosci. 29 2009 179 190
51. Y. Zhang, I.A. Kerman, A. Laque, P. Nguyen, M. Faouzi, G.W. Louis, J.C. Jones, C. Rhodes, and H. Münzberg Leptin-receptor-expressing neurons in the dorsomedial hypothalamus and median preoptic area regulate sympathetic brown adipose tissue circuits J. Neurosci. 31 2011 1873 1884