Altered expression of SOCS3 in the hypothalamic arcuate nucleus during seasonal body mass changes in the field vole, Microtus agrestis

Journal of Neuroendocrinology

Volumn 19, Issue 2, 2007, Pages 83-94

  Król, Elzbieta ^a,b   Tups, A ^a   Archer, Z A ^a   Ross, A W ^a   Moar, K M ^a   Bell, L M ^a   Duncan, J S ^a   Mayer, C ^a   Morgan, P J ^a   Mercer, J G ^a   Speakman, J R ^a,b  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

AgRP; CART; Leptin resistance; NPY; Photoperiod; POMC

Indexed keywords

AGOUTI RELATED PROTEIN; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; LEPTIN; MESSENGER RNA; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ARCUATE NUCLEUS; ARTICLE; BODY MASS; COLD ACCLIMATIZATION; CONTROLLED STUDY; FOOD INTAKE; HORMONE RESISTANCE; HORMONE RESPONSE; HORMONE SENSITIVITY; HYPOTHALAMUS; IN SITU HYBRIDIZATION; MALE; NONHUMAN; OBESITY; PHOTOPERIODICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEASONAL VARIATION; SIGNAL TRANSDUCTION; VOLE;

ACCLIMATIZATION; ANIMALS; ARCUATE NUCLEUS; ARVICOLINAE; BODY WEIGHT; GENE EXPRESSION REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LEPTIN; MALE; NERVE TISSUE PROTEINS; NEUROPEPTIDE Y; PHOTOPERIOD; PRO-OPIOMELANOCORTIN; RNA, MESSENGER; SEASONS; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 33846032327     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2006.01507.x     Document Type: Article

References (81)

1. Stallone DD, Stunkard AJ. The regulation of body weight: Evidence and clinical implications. Ann Behav Med 1991; 13: 220-230.
2. Rosenbaum M, Leibel RL, Hirsch J. Obesity. N Engl J Med 1997; 337: 396-407.
3. Schwartz MW, Seeley RJ. The new biology of body weight regulation. J Am Diet Assoc 1997; 97: 54-58.
4. Levin BE, Keesey RE. Defense of differing body weight set points in diet-induced obese and resistant rats. Am J Physiol Regul Integr Comp Physiol 1998; 274: R412-R419.
5. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 2000; 404: 661-671.
6. Heldmaier G, Steinlechner S. Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 1981; 142: 429-437.
7. Stebbins LL. Overwintering activity of Peromyscus maniculatus Clethrionomys gapperi, C. rutilus, Eutamias amoenus and Microtus pennsylvanicus. In: Merritt J, eds. Winter Ecology of Small Mammals. Pittsburgh, PA: Special Publication of Carnegie Museum Natural History, 1984; 10: 201-213.
8. Bronson FH, Heideman PD. Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. New York: Raven Press, 1994: 541-584.
9. Bartness TJ, Demas GE, Song CK. Seasonal changes in adiposity: The roles of photoperiod, melatonin and other hormones, and sympathetic nervous system. Exp Biol Med 2002; 227: 363-376.
10. Steinlechner S, Heldmaier G. Role of photoperiod and melatonin in seasonal acclimatization of the Djungarian hamster, Phodopus sungorus. Int J Biometeorol 1982; 26: 329-337.
11. Darrow JM, Goldman BD. Circadian regulation of pineal melatonin and reproduction in the Djungarian hamster. J Biol Rhythms 1985; 1: 39-54.
12. Morgan PJ, Ross AW, Mercer JG, Barrett P. Photoperiodic programming of body weight through the neuroendocrine hypothalamus. J Endocrinol 2003; 177: 27-34.
13. Mercer JG, Speakman JR. Hypothalamic neuropeptide mechanisms for regulating energy balance: From rodent models to human obesity. Neurosci Biobehav Rev 2001; 25: 101-116.
14. Rousseau K, Atcha Z, Loudon AS. Leptin and seasonal mammals. J Neuroendocrinol 2003; 15: 409-414.
15. Schuhler S, Ebling FJ. Role of melanocortin in the long-term regulation of energy balance: Lessons from a seasonal model. Peptides 2006; 27: 301-309.
16. Kennedy GC. The role of depot fat in the hypothalamic control of food intake in the rat. Proc R Soc Lond B 1953; 140: 578-592.
17. Elmquist JK, Elias CF, Saper CB. From lesions to leptin: Hypothalamic control of food intake and body weight. Neuron 1999; 22: 221-232.
18. Ahima RS, Saper CB, Flier JS, Elmquist JK. Leptin regulation of neuroendocrine systems. Front Neuroendocrinol 2000; 21: 263-307.
19. Mercer JG, Hoggard N, Williams LM, Lawrence CB, Hannah LT, Morgan PJ, Trayhurn P. Coexpression of leptin receptor and preproneuropeptide Y mRNA in arcuate nucleus of mouse hypothalamus. J Neuroendocrinol 1996; 8: 733-735.
20. Mercer JG, Moar KM, Rayner DV, Trayhurn P, Hoggard N. Regulation of leptin receptor and NPY gene expression in hypothalamus of leptin-treated obese (ob/ob) and cold-exposed lean mice. FEBS Lett 1997; 402: 185-188.
21. Kalra SP, Kalra PS. Overlapping and interactive pathways regulating appetite and craving. J Addict Dis 2004; 23: 5-21.
22. Broberger C, Johansen J, Johansson C, Schalling M, Hokfelt T. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc Natl Acad Sci USA 1998; 95: 15043-15048.
23. Hahn TM, Breininger JF, Baskin DG, Schwartz MW. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1998; 1: 271-272.
24. Kristensen P, Judge ME, Thim L, Ribel U, Christjansen KN, Wulff BS, Clausen JT, Jensen PB, Madsen OD, Vrang N, Larsen PJ, Hastrup S. Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 1998; 393: 72-76.
25. Tritos NA, Vicent D, Gillette J, Ludwig DS, Flier ES, Maratos-Flier E. Functional interactions between melanin-concentrating hormone, neuropeptide Y, and anorectic neuropeptides in the rat hypothalamus. Diabetes 1998; 47: 1687-1692.
26. Abbott CR, Rossi M, Wren AM, Murphy KG, Kennedy AR, Stanley SA, Zollner AN, Morgan DG, Morgan I, Ghatei MA, Small CJ, Bloom SR. Evidence of an orexigenic role for cocaine- and amphetamine-regulated transcript after administration into discrete hypothalamic nuclei. Endocrinology 2001; 142: 3457-3463.
27. Berthoud HR. Multiple neural systems controlling food intake and body weight. Neurosci Biobehav Rev 2002; 26: 393-428.
28. Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: Evidence for diet-induced resistance to leptin action. Nat Med 1995; 1: 1311-1314.
29. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996; 334: 292-295.
30. Zhang Y, Scarpace PJ. Circumventing central leptin resistance. Lessons from central leptin and POMC gene delivery. Peptides 2006; 27: 350-364.
31. Drazen DL, Kriegsfeld LJ, Schneider JE, Nelson RJ. Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. Am J Physiol Regul Integr Comp Physiol 2000; 278: R1401-R1407.
32. Concannon P, Levac K, Rawson R, Tennant B, Bensadoun A. Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am J Physiol Regul Integr Comp Physiol 2001; 281: R951-R959.
33. Johnson MS, Onorato DP, Gower BA, Nagy TR. Weight change affects serum leptin and corticosterone in the collared lemming. Gen Comp Endocrinol 2004; 136: 30-36.
34. Li XS, Wang DH. Regulation of body weight and thermogenesis in seasonally acclimatized Brandt's voles (Microtus brandti) Horm Behav 2005; 48: 321-328.
35. Bjørbaek C, Elmquist JK, Frantz JD, Shoelson SE, Flier JS. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol Cell 1998; 1: 619-625.
36. Dunn SL, Bjornholm M, Bates SH, Chen Z, Seifert M, Myers MG Jr. Feedback inhibition of leptin receptor/Jak2 signaling via Tyr1138 of the leptin receptor and suppressor of cytokine signaling 3. Mol Endocrinol 2005; 19: 925-938.
37. Münzberg H, Myers MG Jr. Molecular and anatomical determinants of central leptin resistance. Nat Neurosci 2005; 8: 566-570.
38. Bjørbaek C, El-Haschimi K, Frantz JD, Flier JS. The role of SOCS-3 in leptin signaling and leptin resistance. J Biol Chem 1999; 274: 30059-30065.
39. Krebs DL, Hilton DJ. SOCS proteins: Negative regulators of cytokine signaling. Stem Cells 2001; 19: 378-387.
40. Mori H, Hanada R, Hanada T, Aki D, Mashima R, Nishinakamura H, Torisu T, Chien KR, Yasukawa H, Yoshimura A. Socs3 deficiency in the brain elevates leptin sensitivity and confers resistance to diet-induced obesity. Nat Med 2004; 10: 739-743.
41. Howard JK, Cave BJ, Oksanen LJ, Tzameli I, Bjørbaek C, Flier JS. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat Med 2004; 10: 734-738.
42. Münzberg H, Flier JS, Bjørbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 2004; 145: 4880-4889.
43. Scarpace PJ, Matheny M, Zhang Y, Shek EW, Prima V, Zolotukhin S, Tumer N. Leptin-induced leptin resistance reveals separate roles for the anorexic and thermogenic responses in weight maintenance. Endocrinology 2002; 143: 3026-3035.
44. Peralta S, Carrascosa JM, Gallardo N, Ros M, Arribas C. Ageing increases SOCS-3 expression in rat hypothalamus: Effects of food restriction. Biochem Biophys Res Commun 2002; 296: 425-428.
45. Mercer JG, Tups A. Neuropeptides and anticipatory changes in behaviour and physiology: Seasonal body weight regulation in the Siberian hamster. Eur J Pharmacol 2003; 480: 43-50.
46. Tups A, Ellis C, Moar KM, Logie TJ, Adam CL, Mercer JG, Klingenspor M. Photoperiodic regulation of leptin sensitivity in the Siberian hamster, Phodopus sungorus, is reflected in arcuate nucleus SOCS-3 (suppressor of cytokine signaling) gene expression. Endocrinology 2004; 145: 1185-1193.
47. Tups A, Barrett P, Ross AW, Morgan PJ, Klingenspor M, Mercer JG. The suppressor of cytokine signalling 3, SOCS3, may be one critical modulator of seasonal body weight changes in the Siberian hamster, Phodopus sungorus. J Neuroendocrinol 2006; 18: 139-145.
48. Król E, Redman P, Thomson PJ, Williams R, Mayer C, Mercer JG, Speakman JR. Effect of photoperiod on body mass, food intake and body composition in the field vole, Microtus agrestis. J Exp Biol 2005; 208: 571-584.
49. Król E, Duncan JS, Redman P, Morgan PJ, Mercer JG, Speakman JR. Photoperiod regulates leptin sensitivity in field voles, Microtus agrestis. J Comp Physiol B 2006; 176: 153-163.
50. Larkin JE, Freeman DA, Zucker I. Low ambient temperature accelerates short-day responses in Siberian hamsters by altering responsiveness to melatonin. J Biol Rhythms 2001; 16: 76-86.
51. Mustonen A-M, Nieminen P, Hyvärinen H. Melatonin and the wintering strategy of the tundra vole, Microtus oeconomus. Zool Sci 2002; 19: 683-687.
52. Nieminen P, Lindström-Seppä P, Mustonen A-M, Mussalo-Rauhamaa H, Kukkonen JVK. Bisphenol A affects endocrine physiology and biotransformation enzyme activities of the field vole (Microtus agrestis). Gen Comp Endocrinol 2002; 126: 183-189.
53. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162: 156-159.
54. Trayhurn P, Duncan JS, Nestor A, Thomas ME, Rayner DV. Chemiluminescent detection of mRNAs on northern blots with digoxigenin end-labeled oligonucleotides. Anal Biochem 1994; 222: 224-230.
55. Trayhurn P, Duncan JS, Rayner DV. Acute cold-induced suppression of ob (obese) gene expression in white adipose tissue of mice: Mediation by the sympathetic system. Biochem J 1995; 311: 729-733.
56. Simmons DM, Arriza JL, Swanson LW. A complete protocol for in situ hybridisation of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA probes. J Histotechnol 1989; 12: 169-181.
57. Mercer JG, Lawrence CB, Beck B, Burlet A, Atkinson T, Barrett P. Hypothalamic NPY and prepro-NPY mRNA in Djungarian hamsters: Effects of food deprivation and photoperiod. Am J Physiol Regul Integr Comp Physiol 1995; 269: R1099-R1106.
58. Mercer JG, Lawrence CB, Moar KM, Atkinson T, Barrett P. Short-day weight loss and effect of food deprivation on hypothalamic NPY and CRF mRNA in Djungarian hamsters. Am J Physiol Regul Integr Comp Physiol 1997; 273: R768-R776.
59. Mercer JG, Moar KM, Ross AW, Hoggard N, Morgan PJ. Photoperiod regulates arcuate nucleus POMC, AGRP, and leptin receptor mRNA in Siberian hamster hypothalamus. Am J Physiol Regul Integr Comp Physiol 2000; 278: R271-R281.
60. Adam CL, Moar KM, Logie TJ, Ross AW, Barrett P, Morgan PJ, Mercer JG. Photoperiod regulates growth, puberty and hypothalamic neuropeptide and receptor gene expression in female Siberian hamsters. Endocrinology 2000; 141: 4349-4356.
61. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1997.
62. Rice WR. Analyzing tables of statistical tests. Evolution 1989; 43: 223-225.
63. Peacock WL, Król E, Moar KM, McLaren JS, Mercer JG, Speakman JR. Photoperiodic effects on body mass, energy balance and hypothalamic gene expression in the bank vole. J Exp Biol 2004; 207: 165-177.
64. Wolden-Hanson T, Marck BT, Smith L, Matsumoto AM. Cross-sectional and longitudinal analysis of age-associated changes in body composition of male Brown Norway rats: Association of serum leptin levels with peripheral adiposity. J Gerontol A Biol Sci Med Sci 1999; 54: B99-B107.
65. Friedman JM, Halaas JL. Leptin and the regulation of body weight in mammals. Nature 1998; 395: 763-770.
66. Woods SC, Schwartz MW, Baskin DG, Seeley RJ. Food intake and the regulation of body weight. Annu Rev Psychol 2000; 51: 255-277.
67. Klingenspor M, Niggemann H, Heldmaier G. Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J Comp Physiol B 2000; 170: 37-43.
68. Atcha Z, Cagampang FR, Stirland JA, Morris ID, Brooks AN, Ebling FJ, Klingenspor M, Loudon AS. Leptin acts on metabolism in a photoperiod-dependent manner, but has no effect on reproductive function in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology 2000; 141: 4128-4135.
69. Lee TM, Spears N, Tuthill CR, Zucker I. Maternal melatonin treatment influences rates of neonatal development of meadow vole pups. Biol Reprod 1989; 40: 495-502.
70. Kriegsfeld LJ, Drazen DL, Nelson RJ. In vitro melatonin treatment enhances cell-mediated immune function in male prairie voles (Microtus ochrogaster). J Pineal Res 2001; 30: 193-198.
71. Steinlechner S, Heldmaier G, Becker H. The seasonal cycle of body weight in the Djungarian hamster: Photoperiodic control and the influence of starvation and melatonin. Oecologia 1983; 60: 401-405.
72. Mercer JG, Moar KM, Logie TJ, Findlay PA, Adam CL, Morgan PJ. Seasonally inappropriate body weight induced by food restriction: Effect on hypothalamic gene expression in male Siberian hamsters. Endocrinology 2001; 142: 4173-4181.
73. Ross AW, Webster CA, Mercer JG, Moar KM, Ebling FJ, Schuhler S, Barrett P, Morgan PJ. Photoperiodic regulation of hypothalamic retinoid signaling: Association of retinoid X receptor gamma with body weight. Endocrinology 2004; 145: 13-20.
74. Ross AW, Bell LM, Littlewood PA, Mercer JG, Barrett P, Morgan PJ. Temporal changes in gene expression in the arcuate nucleus precede seasonal responses in adiposity and reproduction. Endocrinology 2005; 146: 1940-1947.
75. Barrett P, Ross AW, Balik A, Littlewood PA, Mercer JG, Moar KM, Sallmen T, Kaslin J, Panula P, Schuhler S, Ebling FJ, Ubeaud C, Morgan PJ. Photoperiodic regulation of histamine H3 receptor and VGF messenger ribonucleic acid in the arcuate nucleus of the Siberian hamster. Endocrinology 2005; 146: 1930-1939.
76. Tups A, Helwig M, Stohr S, Barrett P, Mercer JG, Klingenspor M. Photoperiodic regulation of insulin receptor mRNA and intracellular insulin signaling in the arcuate nucleus of the Siberian hamster, Phodopus sungorus. Am J Physiol Regul Integr Comp Physiol 2006; 291: R643-R650.
77. Higuchi H, Hasegawa A, Yamaguchi T. Transcriptional regulation of neuronal genes and its effect on neural functions: Transcriptional regulation of neuropeptide Y gene by leptin and its effect on feeding. J Pharmacol Sci 2005; 98: 225-231.
78. Boyer BB, Ormseth OA, Buck L, Nicolson M, Pelleymounter MA, Barnes BM. Leptin prevents posthibernation weight gain but does not reduce energy expenditure in arctic ground squirrels. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1997; 118: 405-412.
79. Robson AJ, Rousseau K, Loudon AS, Ebling FJ. Cocaine and amphetamine-regulated transcript mRNA regulation in the hypothalamus in lean and obese rodents. J Neuroendocrinol 2002; 14: 697-709.
80. Rousseau K, Atcha Z, Cagampang FR, Le Rouzic P, Stirland JA, Ivanov TR, Ebling FJ, Klingenspor M, Loudon AS. Photoperiodic regulation of leptin resistance in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology 2002; 143: 3083-3095.
81. Helwig M, Khorooshi RMH, Tups A, Barrett P, Archer ZA, Exner C, Rozman J, Braulke LJ, Mercer JG, Klingenspor M. PC1/3 and PC2 gene expression and post-translational endoproteolytic pro-opiomelanocortin processing is regulated by photoperiod in the seasonal Siberian hamster (Phodopus sungorus). J Neuroendocrinol 2006; 18: 413-425.