Acute brown adipose tissue temperature response to cold in monosodium glutamate-treated Siberian hamsters

Brain Research

Volumn 1292, Issue , 2009, Pages 38-51

  Leitner, Claudia ^a   Bartness, Timothy J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Agouti related protein; Arcuate nucleus; Lipolysis; Monosodium glutamate; Neuropeptide Y; Obesity; Pseudorabies virus; Thermoregulation

Indexed keywords

GLUTAMATE SODIUM; NEUROPEPTIDE; NORADRENALIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BODY MASS; BROWN ADIPOSE TISSUE; COLD EXPOSURE; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PSEUDORABIES HERPETOVIRUS; STAINING; THALAMUS MIDLINE NUCLEUS; THERMOGENESIS; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; AGING; ANIMALS; ANIMALS, NEWBORN; ARCUATE NUCLEUS; BODY WEIGHT; COLD TEMPERATURE; CRICETINAE; FOOD DEPRIVATION; MALE; NEURAL PATHWAYS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PHODOPUS; SODIUM GLUTAMATE; TEMPERATURE; THERMOGENESIS; TIME FACTORS;

AGOUTI; ANIMALIA; CRICETINAE; SUID HERPESVIRUS 1;

EID: 69449083564     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.07.062     Document Type: Article

References (83)

1. Arch J.R. Central regulation of energy balance: inputs, outputs and leptin resistance. Proc. Nutr. Soc. 64 (2005) 39-46
2. Bai F.L., Yamano M., Shiotani Y., Emson P.C., Smith A.D., Powell J.F., and Tohyama M. An arcuato-paraventricular and -dorsomedial hypothalamic neuropeptide Y-containing neurons in the rat hypothalamus. Brain Res. 331 (1985) 172-175
3. Bamshad M., Aoki V.T., Adkison M.G., Warren W.S., and Bartness T.J. Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am. J. Physiol. 275 (1998) R291-R299
4. Bamshad M., Song C.K., and Bartness T.J. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am. J. Physiol. 276 (1999) R1569-R1578
5. Barrett P., van den Top M., Wilson D., Mercer J.G., Song C.K., Bartness T.J., Morgan P.J., and Spanswick D. Short photoperiod induced decrease of histamine H3 receptors facilitates activation of hypothalamic neurons in the Siberian hamster. Endocrinology (2009)
6. Bartness T.J., and Bamshad M. Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am. J. Physiol. 275 (1998) R1399-R1411
7. Bartness T.J., and Song C.K. Innervation of brown adipose tissue and its role in thermogenesis. Can. J. Diabetes 29 (2005) 420-428
8. Bartness T.J., and Song C.K. Brain-adipose tissue neural crosstalk. Physiol. Behav. 91 (2007) 343-351
9. Bartness T.J., and Song C.K. Sympathetic and sensory innervation of white adipose tissue. J. Lipid Res. 48 (2007) 1655-1672
10. Bartness T.J., Elliott J.A., and Goldman B.D. Control of torpor and body weight patterns by a seasonal timer in Siberian hamsters. Am. J. Physiol. 257 (1989) R142-R149
11. Berthoud H.R. Multiple neural systems controlling food intake and body weight. Neurosci. Biobehav. Rev. 26 (2002) 393-428
12. Berthoud H.R., Patterson L.M., Sutton G.M., Morrison C., and Zheng H. Orexin inputs to caudal raphe neurons involved in thermal, cardiovascular, and gastrointestinal regulation. Histochem. Cell Biol. 123 (2005) 147-156
13. Bing C., Pickavance L., Wang Q., Frankish H., Trayhurn P., and Williams G. Role of hypothalamic neuropeptide Y neurons in the defective thermogenic response to acute cold exposure in fatty Zucker rats. Neuroscience 80 (1997) 277-284
14. Bocker H., Steinlechner S., and Heldmaier G. Complete cold substitution of noradrenaline-induced thermogenesis in the Djungarian hamster, Phodopus sungorus. Experientia 38 (1982) 262
15. Brito M.N., Brito N.A., Baro D.J., Song C.K., and Bartness T.J. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148 (2007) 5339-53347
16. Brito N.A., Brito M.N., and Bartness T.J. Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am. J. Physiol., Regul. Integr. Comp. Physiol. 294 (2008) R1445-R1452
17. Bueno A.A., Oyama L.M., Estadella D., Habitante C.A., Bernardes B.S., Ribeiro E.B., and Oller do Nascimento C.M. Lipid metabolism of monosodium glutamate obese rats after partial removal of adipose tissue. Physiol. Res. 54 (2005) 57-65
18. Cannon B., and Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004) 277-359
19. Cano G., Passerin A.M., Schiltz J.C., Card J.P., Morrison S.F., and Sved A.F. Anatomical substrates for the central control of sympathetic outflow to interscapular adipose tissue during cold exposure. J. Comp. Neurol. 460 (2003) 303-326
20. Choi S., Sparks R., Clay M., and Dallman M.F. Rats with hypothalamic obesity are insensitive to central leptin injections. Endocrinology 140 (1999) 4426-4433
21. Chronwall B.M. Anatomy and physiology of the neuroendocrine arcuate nucleus. Peptides 6 (1985) 1-11
22. Cone R.D., Cowley M.A., Butler A.A., Fan W., Marks D.L., and Low M.J. The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int. J. Obes. Relat. Metab. Disord. 25 Suppl. 5 (2001) S63-S67
23. Cowley M.A., Pronchuk N., Fan W., Dinulescu D.M., Colmers W.F., and Cone R.D. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24 (1999) 155-163
24. Dolnikoff M., Martin-Hidalgo A., Machado U.F., Lima F.B., and Herrera E. Decreased lipolysis and enhanced glycerol and glucose utilization by adipose tissue prior to development of obesity in monosodium glutamate (MSG) treated-rats. Int. J. Obes. Relat. Metab. Disord. 25 (2001) 426-433
25. Dolnikoff M.S., Kater C.E., Egami M., de Andrade I.S., and Marmo M.R. Neonatal treatment with monosodium glutamate increases plasma corticosterone in the rat. Neuroendocrinology 48 (1988) 645-649
26. Dulloo A.G., and Young J.B. Effects of monosodium glutamate and gold thioglucose on dietary regulation of sympathetic nervous system activity in rodents. Metabolism 40 (1991) 113-121
27. Ebling F.J., Arthurs O.J., Turney B.W., and Cronin A.S. Seasonal neuroendocrine rhythms in the male Siberian hamster persist after monosodium glutamate-induced lesions of the arcuate nucleus in the neonatal period. J. Neuroendocrinol. 10 (1998) 701-712
28. Flaim K.E., Horowitz J.M., and Horwitz B.A. Functional and anatomical characteristics of the nerve brown adipose tissue interaction in the rat. Pflugers Arch. 365 (1976) 9-14
29. Foster D.O., and Frydman M.L. Brown adipose tissue: the dominant site of nonshivering thermogenesis in the rat. Experientia, Suppl. 32 (1978) 147-151
30. Foster D.O., and Frydman M.L. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can. J. Physiol. Pharm. 57 (1979) 257-270
31. Foster D.O., Depocas F., and Zaror-Behrens G. Unilaterality of the sympathetic innervation of each pad of interscapular brown adipose tissue. Can. J. Physiol. 60 (1982) 107-113
32. Foster D.O., Depocas F., and Zuker M. Heterogeneity of the sympathetic innervation of rat interscapular brown adipose tissue via intercostal nerves. Can. J. Physiol. Pharm. 60 (1982) 747-754
33. Freeman P.H., and Wellman P.J. Brown adipose tissue thermogenesis induced by low level electrical stimulation of hypothalamus in rats. Brain Res. Bull. 18 (1987) 7-11
34. Hakansson M.L., Hulting A.L., and Meister B. Expression of leptin receptor mRNA in the hypothalamic arcuate nucleus - relationship with NPY neurones. NeuroReport 7 (1996) 3087-3092
35. Halvorson I., Gregor L., and Thornhill J.A. Brown adipose tissue thermogenesis is activated by electrical and chemical (l-glutamate) stimulation of the ventromedial hypothalamic nucleus in cold-acclimated rats. Brain Res. 522 (1990) 76-82
36. Heldmaier G., Klaus S., Wiesinger H., Friedrichs U., and Wenzel M. Cold acclimation and thermogenesis. In: Malan A., and Canguilhem B. (Eds). Living in the Cold II (1989), John Libbey Eurotext, Montrouge, France 347-358
37. Himms-Hagen J. Brown adipose tissue and cold-acclimation. In: Trayhurn P., and Nicholls D.G. (Eds). Brown Adipose Tissue (1986), Arnold, London 214-268
38. Himms-Hagen J. Neural control of brown adipose tissue thermogenesis, hypertrophy, and atrophy. Front. Neuroendocinol. 12 (1991) 38-93
39. Iwase M., Ichikawa K., Tashiro K., Iino K., Shinohara N., Ibayashi S., Yoshinari M., and Fujishima M. Effects of monosodium glutamate-induced obesity in spontaneously hypertensive rats vs. Wistar Kyoto rats: serum leptin and blood flow to brown adipose tissue. Hypertens. Res. 23 (2000) 503-510
40. Kobayashi A., Osaka T., Namba Y., Inoue S., and Kimura S. Involvement of sympathetic activation and brown adipose tissue in calcitonin gene-related peptide-induced heat production in the rat. Brain Res. 849 (1999) 196-202
41. Kong W.M., Stanley S., Gardiner J., Abbott C., Murphy K., Seth A., Connoley I., Ghatei M., Stephens D., and Bloom S. A role for arcuate cocaine and amphetamine-regulated transcript in hyperphagia, thermogenesis, and cold adaptation. FASEB J. 17 (2003) 1688-1690
42. Larsen P.J., Mikkelsen J.D., Jessop D., Lightman S.L., and Chowdrey H.S. Neonatal monosodium glutamate treatment alters both the activity and the sensitivity of the rat hypothalamo-pituitary-adrenocortical axis. J. Endocrinol. 141 (1994) 497-503
43. Legradi G., and Lechan R.M. The arcuate nucleus is the major source for neuropeptide Y-innervation of thyrotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Endocrinology 139 (1998) 3262-3270
44. Leitner C., and Bartness T.J. Food deprivation-induced changes in body fat mobilization after neonatal monosodium glutamate treatment. Am. J. Physiol. 294 (2008) R775-R783
45. Leitner C., and Bartness T.J. Sympathetic circuitry to BAT and the response to acute cold in monosodium-glutamate treated Siberian hamsters. Am. J. Physiol. (2008)
46. Madden C.J., and Morrison S.F. Neurons in the paraventricular nucleus of the hypothalamus inhibit sympathetic outflow to brown adipose tissue. Am. J. Physiol., Regul. Integr. Comp. Physiol. 296 (2009) R831-R843
47. Maletinska L., Toma R.S., Pirnik Z., Kiss A., Slaninova J., Haluzik M., and Zelezna B. Effect of cholecystokinin on feeding is attenuated in monosodium glutamate obese mice. Regul. Pept. 136 (2006) 58-63
48. Mercer J.G., Hoggard N., Williams L.M., Lawrence C.B., Hannah L.T., Morgan P.J., and Trayhurn P. Coexpression of leptin receptor and preproneuropeptide Y mRNA in arcuate nucleus of mouse hypothalamus. J. Neuroendocrinol. 8 (1996) 733-735
49. Morimoto A., Murakami N., Nakamori T., and Watanabe T. Suppression of non-shivering thermogenesis in the rat by heat-seeking behaviour during cold exposure. J. Physiol. 380 (1986) 541-549
50. Moriscot A., Rabelo R., and Bianco A.C. Corticosterone inhibits uncoupling protein gene expression in brown adipose tissue. Am. J. Physiol. 265 (1993) E81-E87
51. Morris M.J., Tortelli C.F., Filippis A., and Proietto J. Reduced BAT function as a mechanism for obesity in the hypophagic, neuropeptide Y deficient monosodium glutamate-treated rat. Regul. Pept. 75-76 (1998) 441-447
52. Morrison S.F. Differential control of sympathetic outflow. Am. J. Physiol., Regul. Integr. Comp. Physiol. 281 (2001) R683-R698
53. Moss D., Ma A., and Cameron D.P. Cafeteria feeding promotes diet-induced thermogenesis in monosodium glutamate-treated mice. Metabolism 34 (1985) 1094-1099
54. Moss D., Ma A., and Cameron D.P. Defective thermoregulatory thermogenesis in monosodium glutamate-induced obesity in mice. Metabolism 34 (1985) 626-630
55. Nascimento Curi C.M., Marmo M.R., Egami M., Ribeiro E.B., Andrade I.S., and Dolnikoff M.S. Effect of monosodium glutamate treatment during neonatal development on lipogenesis rate and lipoprotein lipase activity in adult rats. Biochem. Int. 24 (1991) 927-935
56. Nishioka H., Yoshida T., Yoshioka K., and Kondo M. [Studies on the regulation mechanism for sympathetic nervous system activity-using hypothalamic obese mice]. Nippon Naibunpi Gakkai Zasshi 64 (1988) 554-563
57. Oldfield B.J., Giles M.E., Watson A., Anderson C., Colvill L.M., and McKinley M.J. The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat. Neuroscience 110 (2002) 515-526
58. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164 (1969) 719-721
59. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates (2007), Academic Press, New York
60. Pelz K.M., Routman D., Driscoll J.R., Kriegsfeld L.J., and Dark J. Monosodium glutamate-induced arcuate nucleus damage affects both natural torpor and 2DG-induced torpor-like hypothermia in Siberian hamsters. Am. J. Physiol., Regul. Integr. Comp. Physiol. 294 (2008) R255-R265
61. Phelix C.F., and Hartle D.K. Systemic glutamate induces degeneration of a subpopulation of tyrosine hydroxylase-immunoreactive neurons in the rat area postrema. Brain Res. 516 (1990) 335-340
62. Poon T.K., and Cameron D.P. Measurement of oxygen consumption and locomotor activity in monosodium glutamate-induced obesity. Am. J. Physiol. 234 (1978) E532-E534
63. Racek L., Lenhardt L., and Mozes S. Effect of fasting and refeeding on duodenal alkaline phosphatase activity in monosodium glutamate obese rats. Physiol. Res. 50 (2001) 365-372
64. Rehorek A., Kerecsen L., and Muller F. Measurement of tissue catecholamines of obese rats by liquid chromatography and electrochemical detection. Biomed. Biochim. Acta 46 (1987) 823-827
65. Rothwell N.J., and Stock M.J. Neural regulation of thermogenesis. Trends Neurosci. 5 (1982) 124-126
66. Sawchenko P.E. Toward a new neurobiology of energy balance, appetite, and obesity: the anatomists weigh in. J. Comp. Neurol. 402 (1998) 435-441
67. Schoelch C., Hubschle T., Schmidt I., and Nuesslein-Hildesheim B. MSG lesions decrease body mass of suckling-age rats by attenuating circadian decreases of energy expenditure. Am. J. Physiol: Endocrinol. Metab. 283 (2002) E604-E611
68. Song C.K., Vaughan C.H., Keen-Rhinehart E., Harris R.B., Richard D., and Bartness T.J. Melanocortin-4 receptor mRNA expressed in sympathetic outflow neurons to brown adipose tissue: neuroanatomical and functional evidence. Am. J. Physiol. 295 (2008) R417-R428
69. Soumano K., Desbiens S., Rabelo R., Bakopanos E., Camirand A., and Silva J.E. Glucocorticoids inhibit the transcriptional response of the uncoupling protein-1 gene to adrenergic stimulation in a brown adipose cell line. Mol. Cell. Endocrinol. 165 (2000) 7-15
70. Strack A.M., Bradbury M.J., and Dallman M.F. Corticosterone decreases nonshivering thermogenesis and increases lipid storage in brown adipose tissue. Am. J. Physiol. 268 (1995) R183-R191
71. Takasaki Y. Studies on brain lesion by administration of monosodium l-glutamate to mice. I. Brain lesions in infant mice caused by administration of monosodium l-glutamate. Toxicology 9 (1978) 293-305
72. Tamura H., Kamegai J., Shimizu T., Ishii S., Sugihara H., and Oikawa S. Ghrelin stimulates GH but not food intake in arcuate nucleus ablated rats. Endocrinology 143 (2002) 3268-3275
73. Tokuyama K., and Himms-Hagen J. Adrenalectomy prevents obesity in glutamate-treated mice. Am. J. Physiol. 257 (1989) E139-E144
74. Tsukahara F., Uchida Y., Ohba K., Nomoto T., and Muraki T. Defective stimulation of thyroxine 5′-deiodinase activity by cold exposure and norepinephrine in brown adipose tissue of monosodium glutamate-obese mice. Horm. Metab. Res. 29 (1997) 496-500
75. Tsukahara F., Uchida Y., Ohba K., Ogawa A., Yoshioka T., and Muraki T. 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 (1998) 247-249
76. Voss-Andreae A., Murphy J.G., Ellacott K.L., Stuart R.C., Nillni E.A., Cone R.D., and Fan W. Role of the central melanocortin circuitry in adaptive thermogenesis of brown adipose tissue. Endocrinology 148 (2007) 1550-1560
77. Yehuda S., Carasso R.L., and Mostofsky D.I. The facilitative effects of alpha-MSH and melanin on learning, thermoregulation, and pain in neonatal MSG-treated rats. Peptides 12 (1991) 465-469
78. Yoshida T., Nishioka H., Nakamura Y., and Kondo M. Reduced norepinephrine turnover in mice with monosodium glutamate-induced obesity. Metabolism 33 (1984) 1060-1063
79. Yoshida T., Nishioka H., Nakamura Y., Kanatsuna T., and Kondo M. Reduced norepinephrine turnover in brown adipose tissue of pre-obese mice treated with monosodium-l-glutamate. Life Sci. 36 (1985) 931-938
80. Yoshimatsu H., Egawa M., and Bray G.A. Sympathetic nerve activity after discrete hypothalamic injections of l-glutamate. Brain Res. 601 (1993) 121-128
81. Yoshioka K., Yoshida T., and Kondo M. Effect of acute cold-exposure on norepinephrine turnover and thermogenesis in brown adipose tissue and metabolic rate in MSG-induced obese mice. Jpn. J. Physiol. 39 (1989) 957-962
82. Zaretskaia M.V., Zaretsky D.V., Shekhar A., and DiMicco J.A. Chemical stimulation of the dorsomedial hypothalamus evokes non-shivering thermogenesis in anesthetized rats. Brain Res. 928 (2002) 113-125
83. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., and Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 372 (1994) 425-432