Food deprivation-induced changes in body fat mobilization after neonatal monosodium glutamate treatment

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 294, Issue 3, 2008, Pages

  Leitner, Claudia ^a   Bartness, Timothy J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Agouti related protein; Neuropeptide Y; Sympathetic nervous system; Tyrosine hydroxylase; White adipose tissue

Indexed keywords

AGOUTI RELATED PROTEIN; GLUTAMATE SODIUM; NEUROPEPTIDE Y; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BODY FAT; BODY MASS; BRAIN STEM; CONTROLLED STUDY; DECEREBRATION; FOOD DEPRIVATION; FOOD INTAKE; FOREBRAIN; HUMAN; IMMUNOCOMPETENT CELL; LIPID METABOLISM; NONHUMAN; OBESITY; PHODOPUS; PRIORITY JOURNAL; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE; ANIMALS; ANIMALS, NEWBORN; ARCUATE NUCLEUS; AREA POSTREMA; BODY WEIGHT; CATECHOLAMINES; CELL COUNT; CRICETINAE; EATING; ENERGY METABOLISM; FEMALE; FOOD ADDITIVES; FOOD DEPRIVATION; IMMUNOHISTOCHEMISTRY; LEPTIN; LIPID METABOLISM; NEUROPEPTIDES; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PHODOPUS; SODIUM GLUTAMATE;

EID: 40449096294     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00369.2007     Document Type: Article

References (74)

1. Bai FL, Yamano M, Shiotani Y, Emson PC, Smith AD, Powell JF, Tohyama M. An arcuato-paraventricular and -dorsomedial hypothalamic neuropeptide Y-containing neurons in the rat hypothalamus. Brain Res 331: 172-175, 1985.
2. Bamshad M, Aoki VT, Adkison MG, Warren WS, Bartness TJ. Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. Am J Physiol Regul Integr Comp Physiol 275: R291-R299, 1998.
3. Bartness TJ, Bamshad M. Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am J Physiol Regul Integr Comp Physiol 275: R1399-R1411, 1998.
4. Bartness TJ, Bittman EL, Wade GN. Paraventricular nucleus lesions exaggerate dietary obesity but block photoperiod-induced weight gains and suspension of estrous cyclicity in Syrian hamsters. Brain Res Bull 14: 427-430, 1985.
5. Bartness TJ, Clein MR. Effects of food deprivation and restriction, and metabolic blockers on food hoarding in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 266: R1111-R1117, 1994.
6. Bartness TJ, Demas GE, Song CK. Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormones and the sympathetic nervous system. Exp Biol Med (Maywood) 227: 363-376, 2002.
7. Bartness TJ, Demas GE, Song CK. Central nervous system innervation of white adipose tissue. In: Adipose Tissue, edited by Klaus S. Georgetown, TX: Landes Bioscience, 2001, p. 116-130.
8. Bartness TJ, Hamilton JM, Wade GN, Goldman BD. Regional differences in fat pad responses to short days in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 257: R1533-R1540, 1989.
9. Bartness TJ, Song CK. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res. 48: 1655-1672, 2007.
10. Bartness TJ, Song CK. Brain-adipose tissue neural crosstalk. Physiol Behav 91: 343-351, 2007.
11. Bartness TJ, Song CK, Shi H, Bowers RR, Foster MT. Brain-adipose tissue cross talk. Proc Nutr Soc 64: 53-64, 2005.
12. Baskin DG, Hahn TM, Schwartz MW. Leptin sensitive neurons in the hypothalamus. Horm Metab Res 31: 345-350, 1999.
13. Beck B, Jhanwar-Uniyal M, Burlet A, Chapleur-Chateau M, Leibowitz SF, Burlet C. Rapid and localized alterations of neuropeptide Y (NPY) in discrete hypothalamic nuclei with feeding status. Brain Res 528: 245-249, 1990.
14. Bell ME, Bhatnagar S, Akana SF, Choi S, Dallman MF. Disruption of arcuate/paraventricular nucleus connections changes body energy balance and response to acute stress. J Neurosci 20: 6707-6713, 2000.
15. Bowers RR, Festuccia WTL, Song CK, Shi H, Migliorini RH, Bartness TJ. Sympathetic innervation of white adipose tissue and its regulation of fat cell number. Am J Physiol Regul Integr Comp Physiol 286: R1167-R1175, 2004.
16. Brady LS, Smith MA, Gold PW, Herkenham M. Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 52: 441-447, 1990.
17. Bueno AA, Oyama LM, Estadella D, Habitante CA, Bernardes BS, Ribeiro EB, Oller do Nascimento CM. Lipid metabolism of monosodium glutamate obese rats after partial removal of adipose tissue. Physiol Res 54: 57-65, 2005.
18. Bunyan J, Murrell EA, Shah PP. The induction of obesity in rodents by means of monosodium glutamate. Br J Nutr 35: 25-39, 1976.
19. Choi S, Sparks R, Clay M, Dallman MF. Rats with hypothalamic obesity are insensitive to central leptin injections. Endocrinology 140: 4426-4433, 1999.
20. Cone RD, Cowley MA, Butler AA, Fan W, Marks DL, Low MJ. The arcuate nucleus as a conduit for diverse signals relevant to energy homeostasis. Int J Obes Relat Metab Disord 25, Suppl 5: S63-S67, 2001.
21. Cowley MA, Pronchuk N, Fan W, Dinulescu DM, Colmers WF, Cone RD. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24: 155-163, 1999.
22. Dawson R, Pelleymounter MA, Millard WJ, Liu S, Eppler B. Attenuation of leptin-mediated effects by monosodium glutamate-induced arcuate nucleus damage. Am J Physiol Endocrinol Metab 273: E202-E206, 1997.
23. Djazayery A, Miller DS. The use of gold-thioglucose and monosodium glutamate to induce obesity in mice. Proc Nutr Soc 32: 30A-31A, 1973.
24. 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 278: R1401-R1407, 2000.
25. Ebihara K, Ogawa Y, Katsuura G, Numata Y, Masuzaki H, Satoh N, Tamaki M, Yoshioka T, Hayase M, Matsuoka N, Aizawa-Abe M, Yoshimasa Y, Nakao K. Involvement of agouti-related protein, an endogenous antagonist of hypothalamic melanocortin receptor, in leptin action. Diabetes 48: 2028-2033, 1999.
26. Ebling FJ, Arthurs OJ, Turney BW, Cronin AS. 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: 701-712, 1998.
27. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR, Kuhar MJ, Saper CB, Elmquist JK. Leptin activates hypothalamic CART neurons projections to the spinal cord. Neuron 21: 1375-1385, 1998.
28. Elmquist JK. Hypothalamic pathways underlying the endocrine, autonomic, and behavioral effects of leptin. Int J Obes Relat Metab Disord 25, Suppl 5: S78-S82, 2001.
29. Flegal KM. Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav 86: 599-602, 2005.
30. Giordano A, Song CK, Bowers RR, Ehlen JC, Frontini A, Cinti S, Bartness TJ. White adipose tissue lacks significant vagal innervation and immunohistochemical evidence of parasympathetic innervation. Am J Physiol Regul Integr Comp Physiol 291: R1243-R1255, 2006.
31. Grill HJ, Kaplan JM. The neuroanatomical axis for control of energy balance. Front Neuroendocrinol 23: 2-40, 2002.
32. Hakansson ML, Hulting AL, Meister B. Expression of leptin receptor mRNA in the hypothalamic arcuate nucleus - relationship with NPY neurones. Neuroreport 7: 3087-3092, 1996.
33. Harris RB, Kelso EW, Flatt WP, Bartness TJ, Grill HJ. Energy expenditure and body composition of chronically maintained decerebrate rats in the fed and fasted condition. Endocrinology 147: 1365-1376, 2006.
34. Jones AP, Assimon SA, Gold RM, Sylvan A. Adipose tissue mobilization is unaffected by obesifying hypothalamic knife cuts. Physiol Behav 34: 29-31, 1985.
35. Kanarek RB, Meyers J, Meade RG, Mayer J. Juvenile-onset obesity and deficits in caloric regulation in MSG-treated rats. Pharmacol Biochem Behav 10: 717-721, 1979.
36. Karcsu S, Jancso G, Kreutzberg GW, Toth L, Kiraly E, Bacsy E, Laszlo FA. A glutamate-sensitive neuronal system originating from the area postrema terminates in and transports acetylcholinesterase to the nucleus of the solitary tract. J Neurocytol 14: 563-578, 1985.
37. Koplan JP, Liverman CT, Kraak VI. Preventing childhood obesity: health in the balance: executive summary. J Am Diet Assoc 105: 131-138, 2005.
38. 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 393: 72-76, 1998.
39. Leibowitz SF, Hammer NJ, Chang K. Hypothalamic paraventricular nucleus lesions produce overeating and obesity in the rat. Physiol Behav 27: 1031-1040, 1981.
40. Menendez JA, McGregor IS, Healey PA, Atrens DM, Leibowitz SF. Metabolic effects of neuropeptide Y injections into the paraventricular nucleus of the hypothalamus. Brain Res 516: 8-14, 1990.
41. 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 8: 733-735, 1996.
42. 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 278: R271-R281, 2000.
43. Morris MJ, Tortelli CF, Filippis A, Proietto J. Reduced BAT function as a mechanism for obesity in the hypophagic, neuropeptide Y deficient monosodium glutamate-treated rat. Regul Pept 75-76: 441-447, 1998.
44. Moss D, Ma A, Cameron DP. Defective thermoregulatory thermogenesis in monosodium glutamate-induced obesity in mice. Metabolism 34: 626-630, 1985.
45. Nascimento Curi CM, Marmo MR, Egami M, Ribeiro EB, Andrade IS, Dolnikoff MS. Effect of monosodium glutamate treatment during neonatal development on lipogenesis rate and lipoprotein lipase activity in adult rats. Biochem Int 24: 927-935, 1991.
46. Nikoletseas MM. Obesity in exercising, hypophagic rats treated with monosodium glutamate. Physiol Behav 19: 767-773, 1977.
47. Nishioka H, Yoshida T, Yoshioka K, Kondo M. Studies on the regulation mechanism for sympathetic nervous system activity - using hypothalamic obese mice [In Japanese]. Nippon Naibunpi Gakkai Zasshi 64: 554-563, 1988.
48. Ochi M, Furukawa H, Yoshioka H, Sawada T, Kusunoki T, Hattori T. Adipocyte dynamics in hypothalamic obese mice during food deprivation and refeeding. J Nutr Sci Vitaminol (Tokyo) 37: 479-491, 1991.
49. Ogden CL, Carroll MD, Curtin LR, McDowell MA, Tabak CJ, Flegal KM. Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 295: 1549-1555, 2006.
50. Olney JW. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164: 719-721, 1969.
51. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2001.
52. Perez VJ, Olney JW. Accumulation of glutamic acid in the arcuate nucleus of the hypothalamus of the infant mouse following subcutaneous administration of monosodium glutamate. J Neurochem 19: 1777-1782, 1972.
53. Racek L, Lenhardt L, Mozes S. Effect of fasting and refeeding on duodenal alkaline phosphatase activity in monosodium glutamate obese rats. Physiol Res 50: 365-372, 2001.
54. Rehorek A, Kerecsen L, Muller F. Measurement of tissue catecholamines of obese rats by liquid chromatography and electrochemical detection. Biomed Biochim Acta 46: 823-827, 1987.
55. Remke H, Wilsdorf A, Muller F. Development of hypothalamic obesity in growing rats. Exp Pathol 33: 223-232, 1988.
56. Ribeiro EB, Marmo MR, Andrade IS, Dolnikoff MS. Effect of fasting on monosodium glutamate-obese rats. Braz J Med Biol Res 22: 917-921, 1989.
57. Satcher D. Overweight and obesity threaten U.S. health gains (Online). U.S. Department of Health and Human Services. http://www.asu.edu/educ/ epsl/CERU/Articles/CERU-0112-81-OWI.pdf [2001].
58. Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG. Identification of targets of leptin action in the rat hypothalamus. J Clin Invest 98: 1101-1106, 1996.
59. Shi H, Bartness TJ. Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Res Bull 54: 375-385, 2001.
60. Small CJ, Liu YL, Stanley SA, Connoley IP, Kennedy A, Stock MJ, Bloom SR. Chronic CNS administration of Agouti-related protein (Agrp) reduces energy expenditure. Int J Obes Relat Metab Disord 27: 530-533, 2003.
61. Song CK, Bartness TJ. CNS sympathetic outflow neurons to white fat that express melatonin receptors may mediate seasonal adiposity. Am J Physiol Regul Integr Comp Physiol 281: R666-R672, 2001.
62. Song CK, Jackson RX, Harris RBS, Richard D, Bartness TJ. Melanocortin-4 receptor mRNA is expressed in sympathetic nervous system outflow neurons to white adipose tissue. Am J Physiol Regul Integr Comp Physiol 289: R1467-R1476, 2005.
63. 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: 293-305, 1978.
64. Tamura H, Kamegai J, Shimizu T, Ishii S, Sugihara H, Oikawa S. Ghrelin stimulates GH but not food intake in arcuate nucleus ablated rats. Endocrinology 143: 3268-3275, 2002.
65. Tsukahara F, Uchida Y, Ohba K, Nomoto T, 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: 496-500, 1997.
66. Tsukahara F, Uchida Y, Ohba K, Ogawa A, Yoshioka T, 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: 247-249, 1998.
67. Wade GN, Bartness TJ. Effects of photoperiod and gonadectomy on food intake, body weight and body composition in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 246: R26-R30, 1984.
68. Wood AD, Bartness TJ. Food deprivation-induced increases in hoarding by Siberian hamsters are not photoperiod-dependent. Physiol Behav 60: 1137-1145, 1996.
69. Woods SC, Seeley RJ. Adiposity signals and the control of energy homeostasis. Nutrition 16: 894-902, 2000.
70. Yasuda T, Masaki T, Kakuma T, Yoshimatsu H. Centrally administered ghrelin suppresses sympathetic nerve activity in brown adipose tissue of rats. Neurosci Lett 349: 75-78, 2003.
71. Yoshida T, Nishioka H, Nakamura Y, Kanatsuna T, Kondo M. Reduced norepinephrine turnover in brown adipose tissue of pre-obese mice treated with monosodium-L-glutamate. Life Sci 36: 931-938, 1985.
72. Yoshida T, Nishioka H, Nakamura Y, Kondo M. Reduced norepinephrine turnover in mice with monosodium glutamate-induced obesity. Metabolism 33: 1060-1063, 1984.
73. Yoshida T, Yoshioka K, Nishioka H, Kondo M. Lesions of hypothalamic PVN and norepinephrine turnover in rats. Endocrinol Jpn 36: 187-194, 1989.
74. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432, 1994.