VGF is required for obesity induced by diet, gold thioglucose treatment, and agouti and is differentially regulated in pro-opiomelanocortin- and neuropeptide Y-containing arcuate neurons in response to fasting

Journal of Neuroscience

Volumn 22, Issue 16, 2002, Pages 6929-6938

  Hahm, Seung ^a   Fekete, Csaba ^b,d   Mizuno, Tooru M ^a   Windsor, Joan ^a   Yan, Hai ^f   Boozer, Carol N ^e   Lee, Charlotte ^c   Elmquist, Joel K ^c   Lechan, Ronald M ^d   Mobbs, Charles V ^a   Salton, Stephen R J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c HARVARD MEDICAL SCHOOL   (United States)

^d TUFTS MEDICAL CENTER   (United States)

^e Columbia Univ Coll of Phys/Surg ^*  (United States)

^f AMGEN INC   (United States)

Author keywords

Agouti; Hypothalamus; Leptin; Melanocortin; Neurotrophin; NPY; Obesity; POMC; VGF

Indexed keywords

AGOUTI RELATED PROTEIN; AUROTHIOGLUCOSE; GENE PRODUCT; GLUTAMATE SODIUM; LEPTIN; MELANOCORTIN 4 RECEPTOR; MESSENGER RNA; NEUROPEPTIDE Y; POLYPEPTIDE; PROOPIOMELANOCORTIN; PROTEIN VGF; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BRAIN STEM; DIET RESTRICTION; ENERGY BALANCE; GENE DELETION; GENE EXPRESSION; GENE INDUCTION; GENE TARGETING; HYPOTHALAMUS; MALE; MOUSE; NERVE PROJECTION; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; WEIGHT GAIN;

EID: 0037104786     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-16-06929.2002     Document Type: Article

References (50)

1. Ahima RS, Saper CB, Flier JS, Elmquist JK (2000) Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 21:263-307.
2. Bamshad M, Song CK, Bartness TJ (1999) CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am J Physiol 276:R1569-R1578.
3. Barsh G (1999) From Agouti to Pome: 100 Years of fat blonde mice. Nat Med 5:984-985.
4. Barsh GS, Farooqi IS, O'Rahilly S (2000) Genetics of body-weight regulation. Nature 404:644-651.
5. Bergen HT, Mizuno TM, Taylor J, Mobbs CV (1998) Hyperphagia and weight gain after gold-thioglucose: Relation to hypothalamic neuropeptide Y and proopiomelanocortin. Endocrinology 139:4483-4488.
6. Bonni A, Ginty DD, Dudek H, Greenberg ME (1995) Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals. Mol Cell Neurosci 6:168-183.
7. Chung WK, Belfi K, Chua M, Wiley J, Mackintosh R, Nicolson M, Boozer CN, Leibel RL (1998) Heterozygosity for Lep(ob) or Lep(rdb) affects body composition and leptin homeostasis in adult mice. Am J Physiol 274:R985-R990.
8. D'Arcangelo G, Habas R, Wang S, Halegoua S, Salton SR (1996) Activation of codependent transcription factors is required for transcriptional induction of the vgf gene by nerve growth factor and Ras. Mol Cell Biol 16:4621-4631.
9. Di Rocco G, Pennuto M, Illi B, Canu N, Filocamo G, Trani E, Rinaldi AM, Possenti R, Mandolesi G, Sirinian MI, Jucker R, Levi A, Nasi S (1997) Interplay of the E box, the cyclic AMP response element, and HTF4/HEB in transcriptional regulation of the neurospecific, neurotrophin-inducible vgf gene. Mol Cell Biol 17:1244-1253.
10. Elias CF, Saper CB, Maratos-Flier E, Tritos NA, Lee C, Kelly J, Tatro JB, Hoffman GE, Ollmann MM, Barsh GS, Sakurai T, Yanagisawa M, Elmquist JK (1998) Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J Comp Neurol 402:442-459.
11. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, Flier JS, Saper CB, Elmquist JK (1999) Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23:775-786.
12. Elmquist JK, Elias CF, Saper CB (1999) From lesions to leptin: Hypothalamic control of food intake and body weight. Neuron 22:221-232.
13. Erickson JC, Hollopeter G, Palmiter RD (1996) Attenuation of the obesity syndrome of ob/ob mice by the loss of neuropeptide Y. Science 274:1704-1707.
14. Fan W, Boston BA, Kesterson RA, Hruby VJ, Cone RD (1997) Role of melanocortinergic neurons in feeding and the agouti obesity syndrome. Nature 385:165-168.
15. Fekete C, Legradi G, Mihaly E, Huang QH, Tatro JB, Rand WM, Emerson CH, Lechan RM (2000a) α-melanocyte-stimulating hormone is contained in nerve terminals innervating thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and prevents fasting-induced suppression of prothyrotropin-releasing hormone gene expression. J Neurosci 20:1550-1558.
16. Fekete C, Mihaly E, Luo LG, Kelly J, Clausen JT, Mao Q, Rand WM, Moss LG, Kuhar M, Emerson CH, Jackson IM, Lechan RM (2000b) Association of cocaine- and amphetamine-regulated transcript-immunoreactive elements with thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus and its role in the regulation of the hypothalamic-pituitary-thyroid axis during fasting. J Neurosci 20:9224-9234.
17. Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763-770.
18. Grill HJ, Ginsberg AB, Seeley RJ, Kaplan JM (1998) Brainstem application of melanocortin receptor ligands produces long-lasting effects on feeding and body weight. J Neurosci 18:10128-10135.
19. Gunn TM, Miller KA, He L, Hyman RW, Davis RW, Azarani A, Schlossman SF, Duke-Cohan JS, Barsh GS (1999) The mouse mahogany locus encodes a transmembrane form of human attractin. Nature 398:152-156.
20. Hahm S, Mizuno TM, Wu TJ, Wisor JP, Priest CA, Kozak CA, Boozer CN, Peng B, McEvoy RC, Good P, Kelley KA, Takahashi JS, Pintar JE, Roberts JL, Mobbs CV, Salton SR (1999) Targeted deletion of the Vgf gene indicates that the encoded secretory peptide precursor plays a novel role in the regulation of energy balance. Neuron 23:537-548.
21. Hahn TM, Breininger JF, Baskin DG, Schwartz MW (1998) Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1:271-272.
22. Hawley RJ, Scheibe RJ, Wagner JA (1992) NGF induces the expression of the VGF gene through a cAMP response element. J Neurosci 12:2573-2581.
23. Hollopeter G, Erickson JC, Palmiter RD (1998) Role of neuropeptide Y in diet-, chemical-, and genetic-induced obesity of mice. Int J Obes Relat Metab Disord 22:506-512.
24. Kanemasa K, Okamura H, Kodama T, Ibata Y (1995a) Induction of VGF mRNA in neurons of the rat nucleus tractus solitarius and the dorsal motor nucleus of vagus in duodenal ulceration by cysteamine. Brain Res Mol Brain Res 32:55-62.
25. Kanemasa K, Okamura H, Kodama T, Kashima K, Ibata Y (1995b) Time course of the induction of VGF mRNA in the dorsal vagal complex in rats with cysteamine-induced peptic ulcers. Brain Res Mol Brain Res 34:309-314.
26. Legradi G, Lechan RM (1998) The arcuate nucleus is the major source for neuropeptide Y-innervation of thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 139:3262-3270.
27. Legradi G, Lechan RM (1999) Agouti-related protein containing nerve terminals innervate thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 140:3643-3652.
28. Legradi G, Emerson CH, Ahima RS, Rand WM, Flier JS, Lechan RM (1998) Arcuate nucleus ablation prevents fasting-induced suppression of ProTRH mRNA in the hypothalamic paraventricular nucleus. Neuroendocrinology 68:89-97.
29. Luc PV, Wagner JA (1997) Regulation of the neural-specific gene VGF in PC12 cells. Identification of transcription factors interacting with NGF-responsive elements. J Mol Neurosci 8:223-241.
30. Miller MW, Duhl DM, Vrieling H, Cordes SP, Ollmann MM, Winkes BM, Barsh GS (1993) Cloning of the mouse agouti gene predicts a secreted protein ubiquitously expressed in mice carrying the lethal yellow mutation. Genes Dev 7:454-467.
31. Mizuno TM, Mobbs CV (1999) Hypothalamic agouti-related protein messenger ribonucleic acid is inhibited by leptin and stimulated by fasting. Endocrinology 140:814-817.
32. Mizuno TM, Bergen H, Kleopoulos S, Bauman WA, Mobbs CV (1996a) Effects of nutritional status and aging on leptin gene expression in mice: Importance of glucose. Horm Metab Res 28:679-684.
33. Mizuno TM, Bergen H, Funabashi T, Kleopoulos SP, Zhong YG, Bauman WA, Mobbs CV (1996b) Obese gene expression: Reduction by fasting and stimulation by insulin and glucose in lean mice, and persistent elevation in acquired (diet-induced) and genetic (yellow agouti) obesity. Proc Natl Acad Sci USA 93:3434-3438.
34. Mizuno TM, Kleopoulos SP, Bergen HT, Roberts JL, Priest CA, Mobbs CV (1998) Hypothalamic pro-opiomelanocortin mRNA is reduced by fasting and [corrected] in ob/ob and db/db mice, but is stimulated by leptin. Diabetes 47:294-297.
35. Mizuno TM, Makimura H, Silverstein J, Roberts JL, Lopingco T, Mobbs CV (1999) Fasting regulates hypothalamic neuropeptide Y, agoutirelated peptide, and proopiomelanocortin in diabetic mice independent of changes in leptin or insulin. Endocrinology 140:4551-4557.
36. Morris MJ, Tortelli CF, Filippis A, Proietto J (1998) Reduced BAT function as a mechanism for obesity in the hypophagic, neuropeptide Y-deficient monosodium glutamate-treated rat. Regul Pept 75-76:441-447.
37. Morrison SF (2001a) Differential control of sympathetic outflow. Am J Physiol Regul Integr Comp Physiol 281:R683-R698.
38. Morrison SF (2001b) Differential regulation of sympathetic outflows to vasoconstrictor and thermoregulatory effectors. Ann NY Acad Sci 940:286-298.
39. Mountjoy KG, Mortrud MT, Low MJ, Simerly RB, Cone RD (1994) Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 8:1298-1308.
40. Nagle DL, McGrail SH, Vitale J, Woolf EA, Dussault Jr BJ, DiRocco L, Holmgren L, Montagno J, Bork P, Huszar D, Fairchild-Huntress V, Ge P, Keilty J, Ebeling C, Baldini L, Gilchrist J, Burn P, Carlson GA, Moore KJ (1999) The mahogany protein is a receptor involved in suppression of obesity. Nature 398:148-152.
41. Palkovits M (1999) Interconnections between the neuroendocrine hypothalamus and the central autonomic system. Geoffrey Harris Memorial Lecture, Kitakyushu, Japan, October 1998. Front Neuroendocrinol 20:270-295.
42. Pizzi WJ, Barnhart JE (1976) Effects of monosodium glutamate on somatic development, obesity, and activity in the mouse. Pharmacol Biochem Behav 5:551-557.
43. Salton SR, Volonte C, D'Arcangelo G (1995) Stimulation of vgf gene expression by NGF is mediated through multiple signal transduction pathways involving protein phosphorylation. FEBS Lett 360:106-110.
44. Salton SR, Hahm S, Mizuno TM (2000a) Of mice and MEN: What transgenic models tell us about hypothalamic control of energy balance. Neuron 25:265-268.
45. Salton SR, Ferri GL, Hahm S, Snyder SE, Wilson AJ, Possenti R, Levi A (2000b) VGF: A novel role for this neuronal and neuroendocrine polypeptide in the regulation of energy balance. Front Neuroendocrinol 21:199-219.
46. Sawchenko PE, Swanson LW (1982) Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260-272.
47. Schwartz MW, Woods SC, Porte Jr D, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661-671.
48. Shimizu-Albergine M, Ippolito DL, Beavo JA (2001) Downregulation of fasting-induced cAMP response element-mediated gene induction by leptin in neuropeptide Y neurons of the arcuate nucleus. J Neurosci 21:1238-1246.
49. Tsukahara F, Uchida Y, Ohba K, Ogawa A, Yoshioka T, Muraki T (1998) The effect of acute cold exposure and norepinephrine on uncoupling protein gene expression in brown adipose tissue of monosodium glutamate-obese mice. Jpn J Pharmacol 77:247-249.
50. van der Kraan M, Tatro JB, Entwistle ML, Brakkee JH, Burbach JP, Adan RA, Gispen WH (1999) Expression of melanocortin receptors and pro-opiomelanocortin in the rat spinal cord in relation to neurotrophic effects of melanocortins. Brain Res Mol Brain Res 63:276-286.