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Experimental Diabetes Research
Volume 2011, Article ID 947917, 11 pages
http://dx.doi.org/10.1155/2011/947917
Research Article

Impaired Sympathoadrenal Axis Function Contributes to Enhanced Insulin Secretion in Prediabetic Obese Rats

1Laboratory of Physiology, Department of Physiology, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil
2Laboratory of Secretion Cell Biology, Department of Cell Biology and Genetics, State University of Maringá, 87020-900 Maringá, PR, Brazil
3Laboratory of Cell Biology, Department of Biology, Federal University of Juiz de Fora, 36036-900 Juiz de Fora, MG, Brazil

Received 14 April 2011; Accepted 13 June 2011

Academic Editor: Stavros Liatis

Copyright © 2011 Ana Eliza Andreazzi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T. Coll, R. Rodríguez-Calvo, E. Barroso et al., “Peroxisome proliferator-activated receptor (PPAR) β/δ: a new potential therapeutic target for the treatment of metabolic syndrome,” Current Molecular Pharmacology, vol. 2, no. 1, pp. 46–55, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. J. De Flines and A. J. Scheen, “Management of metabolic syndrome and associated cardiovascular risk factors,” Acta gastro-enterologica Belgica, vol. 73, no. 2, pp. 261–266, 2010. View at Google Scholar · View at Scopus
  3. C. Vernochet, S. B. Peres, and S. R. Farmer, “Mechanisms of obesity and related pathologies: transcriptional control of adipose tissue development,” FEBS Journal, vol. 276, no. 20, pp. 5729–5737, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. H. R. Berthoud and C. Morrison, “The brain, appetite, and obesity,” Annual Review of Psychology, vol. 59, pp. 55–92, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. G. Williams, C. Bing, X. J. Cai, J. A. Harrold, P. J. King, and X. H. Liu, “The hypothalamus and the control of energy homeostasis: different circuits, different purposes,” Physiology and Behavior, vol. 74, no. 4-5, pp. 683–701, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Abizaid and T. L. Horvath, “Brain circuits regulating energy homeostasis,” Regulatory Peptides, vol. 149, no. 1–3, pp. 3–10, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. S. Obici, “Minireview: molecular targets for obesity therapy in the brain,” Endocrinology, vol. 150, no. 6, pp. 2512–2517, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. H. Yoshimatsu, M. Egawa, and G. A. Bray, “Sympathetic nerve activity after discrete hypothalamic injections of L-glutamate,” Brain Research, vol. 601, no. 1-2, pp. 121–128, 1993. View at Publisher · View at Google Scholar · View at Scopus
  9. Q. Gao and T. L. Horvath, “Neuronal control of energy homeostasis,” FEBS Letters, vol. 582, no. 1, pp. 132–141, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. K. P. Davy and J. S. Orr, “Sympathetic nervous system behavior in human obesity,” Neuroscience and Biobehavioral Reviews, vol. 33, no. 2, pp. 116–124, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. K. L. Teff, “Visceral nerves: vagal and sympathetic innervation,” Journal of Parenteral and Enteral Nutrition, vol. 32, no. 5, pp. 569–571, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. E. Ravussin and P. A. Tataranni, “The role of altered sympathetic nervous system activity in the pathogenesis of obesity,” Proceedings of the Nutrition Society, vol. 55, no. 3, pp. 793–802, 1996. View at Google Scholar · View at Scopus
  13. N. Tentolouris, G. Argyrakopoulou, and N. Katsilambros, “Perturbed autonomic nervous system function in metabolic syndrome,” NeuroMolecular Medicine, vol. 10, no. 3, pp. 169–178, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. G. A. Bray, D. A. York, and J. S. Fisler, “Experimental obesity: a homeostatic failure due to defective nutrient stimulation of the sympathetic nervous system,” Vitamins and Hormones, vol. 45, pp. 1–125, 1989. View at Publisher · View at Google Scholar · View at Scopus
  15. G. A. Bray, “Obesity, a disorder of nutrient partitioning: the MONA LISA hypothesis,” Journal of Nutrition, vol. 121, no. 8, pp. 1146–1162, 1991. View at Google Scholar · View at Scopus
  16. J. B. Young, “Developmental origins of obesity: a sympathoadrenal perspective,” International Journal of Obesity, vol. 30, no. 4, pp. S41–S49, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. F. Sala, A. Nistri, and M. Criado, “Nicotinic acetylcholine receptors of adrenal chromaffin cells,” Acta Physiologica, vol. 192, no. 2, pp. 203–212, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. J. E. Silva and S. D. C. Bianco, “Thyroid-adrenergic interactions: physiological and clinical implications,” Thyroid, vol. 18, no. 2, pp. 157–165, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. S. Schenk, M. Saberi, and J. M. Olefsky, “Insulin sensitivity: modulation by nutrients and inflammation,” Journal of Clinical Investigation, vol. 118, no. 9, pp. 2992–3002, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. M. Lee and J. Korner, “Review of physiology, clinical manifestations, and management of hypothalamic obesity in humans,” Pituitary, vol. 12, no. 2, pp. 87–95, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. D. X. Scomparin, S. Grassiolli, A. C. Marçal, C. Gravena, A. E. Andreazzi, and P. C. F. Mathias, “Swim training applied at early age is critical to adrenal medulla catecholamine content and to attenuate monosodium l-glutamate-obesity onset in mice,” Life Sciences, vol. 79, no. 22, pp. 2151–2156, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. L. L. Bernardis and B. D. Patterson, “Correlation between “Lee index” and carcass fat content in weanling and adult female rats with hypothalamic lesions,” Journal of Endocrinology, vol. 40, no. 4, pp. 527–528, 1968. View at Google Scholar · View at Scopus
  23. T. Leon-Quinto, C. Magnan, and B. Portha, “Altered activity of the autonomous nervous system as a determinant of the impaired β-cell secretory response after protein-energy restriction in the rat,” Endocrinology, vol. 139, no. 8, pp. 3382–3389, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. K. L. Kelner, R. A. Levine, K. Morita, and H. B. Pollard, “A comparison of trihydroxyindole and HPLC/electrochemical methods for catecholamine measurement in adrenal chromaffin cells,” Neurochemistry International, vol. 7, no. 2, pp. 373–378, 1985. View at Publisher · View at Google Scholar · View at Scopus
  25. A. C. P. Martins, K. L. A. Souza, M. T. Shio, P. C. F. Mathias, P. I. Lelkes, and R. M. G. Garcia, “Adrenal medullary function and expression of catecholamine-synthesizing enzymes in mice with hypothalamic obesity,” Life Sciences, vol. 74, no. 26, pp. 3211–3222, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Google Scholar · View at Scopus
  27. A. M. Krstulovic, “Investigations of catecholamine metabolism using high-performance liquid chromatography. Analytical methodology and clinical applications,” Journal of Chromatography, vol. 229, no. 1, pp. 1–34, 1982. View at Google Scholar · View at Scopus
  28. A. M. Scott, I. Atwater, and E. Rojas, “A method for the simultaneous measurement of insulin release and B cell membrane potential in single mouse islets of Langerhans,” Diabetologia, vol. 21, no. 5, pp. 470–475, 1981. View at Google Scholar · View at Scopus
  29. M. P. Hermans, W. Schmeer, and J. C. Henquin, “Modulation of the effect of acetylcholine on insulin release by the membrane potential on B cells,” Endocrinology, vol. 120, no. 5, pp. 1765–1773, 1987. View at Google Scholar · View at Scopus
  30. S. Grassiolli, M. L. Bonfleur, D. X. Scomparin, and P. C. De Freitas Mathias, “Pancreatic islets from hypothalamic obese rats maintain K+ATP channel-dependent but not -independent pathways on glucose-induced insulin release process,” Endocrine, vol. 30, no. 2, pp. 191–196, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. A. C. Marçal, S. Grassiolli, D. N. Da Rocha et al., “The dual effect of isoproterenol on insulin release is suppressed in pancreatic islets from hypothalamic obese rats,” Endocrine, vol. 29, no. 3, pp. 445–449, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Sieg, J. Su, A. Muñoz et al., “Epinephrine-induced hyperpolarization of islet cells without K ATP channels,” American Journal of Physiology, vol. 286, no. 3, pp. E463–E471, 2004. View at Google Scholar · View at Scopus
  33. J. Bunyan, E. A. Murrell, and P. P. Shah, “The induction of obesity in rodents by means of monosodium glutamate,” British Journal of Nutrition, vol. 35, no. 1, pp. 25–39, 1976. View at Google Scholar · View at Scopus
  34. J. W. Olney, “Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate,” Science, vol. 164, no. 3880, pp. 719–721, 1969. View at Google Scholar · View at Scopus
  35. M. Dolnikoff, A. Martín-Hidalgo, U. F. Machado, F. B. Lima, and E. Herrera, “Decreased lipolysis and enhanced glycerol and glucose utilization by adipose tissue prior to development of obesity in monosodium glutamate (MSG) treated-rats,” International Journal of Obesity, vol. 25, no. 3, pp. 426–433, 2001. View at Publisher · View at Google Scholar · View at PubMed
  36. S. Balbo, S. Grassiolli, R. Ribeiro et al., “Fat storage is partially dependent on vagal activity and insulin secretion of hypothalamic obese rat,” Endocrine, vol. 31, no. 2, pp. 142–148, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Grassiolli, C. Gravena, and P. C. de Freitas Mathias, “Muscarinic M2 receptor is active on pancreatic islets from hypothalamic obese rat,” European Journal of Pharmacology, vol. 556, no. 1–3, pp. 223–228, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. D. Maiter, L. E. Underwood, J. B. Martin, and J. I. Koenig, “Neonatal treatment with monosodium glutamate: effects of prolonged growth hormone (GH)-releasing hormone deficiency on pulsatile GH secretion and growth in female rats,” Endocrinology, vol. 128, no. 2, pp. 1100–1106, 1991. View at Google Scholar · View at Scopus
  39. J. B. Young and L. Landsberg, “Diminished sympathetic nervous system activity in genetically obese (ob/ob) mouse,” The American journal of physiology, vol. 245, no. 2, pp. E148–E154, 1983. View at Google Scholar · View at Scopus
  40. B. E. Levin, “Reduced norepinephrine turnover in organs and brains of obesity-prone rats,” American Journal of Physiology, vol. 268, no. 2, pp. R389–R394, 1995. View at Google Scholar · View at Scopus
  41. M. F. Saad, S. A. Alger, F. Zurlo, J. B. Young, C. Bogardus, and E. Ravussin, “Ethnic differences in sympathetic nervous system-mediated energy expenditure,” American Journal of Physiology, vol. 261, no. 6, pp. E789–E794, 1991. View at Google Scholar · View at Scopus
  42. K. P. Davy and J. E. Hall, “Obesity and hypertension: two epidemics or one?” American Journal of Physiology, vol. 286, no. 5, pp. R803–R813, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. T. Yoshida, K. Yoshioka, N. Hiraoka, and M. Kondo, “Effect of nicotine on norepinephrine turnover and thermogenesis in brown adipose tissue and metabolic rate in MSG obese mice,” Journal of Nutritional Science and Vitaminology, vol. 36, no. 2, pp. 123–130, 1990. View at Google Scholar · View at Scopus
  44. I. S. de Andrade, J. C. G. Gonzalez, A. E. Hirata et al., “Central but not peripheral glucoprivation is impaired in monosodium glutamate-treated rats,” Neuroscience Letters, vol. 398, no. 1-2, pp. 6–11, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. A. E. Andreazzi, D. X. Scomparin, F. P. Mesquita et al., “Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice,” Journal of Endocrinology, vol. 201, no. 3, pp. 351–359, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. J. B. Young and I. A. MacDonald, “Sympathoadrenal activity in human obesity: heterogeneity of findings since 1980,” International Journal of Obesity, vol. 16, no. 12, pp. 959–967, 1992. View at Google Scholar
  47. A. Astrup, “The sympathetic nervous system as a target for intervention in obesity,” International Journal of Obesity, vol. 19, supplement 7, pp. S24–S28, 1995. View at Google Scholar
  48. J. B. Young, “Programming of sympathoadrenal function,” Trends in Endocrinology and Metabolism, vol. 13, no. 9, pp. 381–385, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. J. W. E. Jocken and E. E. Blaak, “Catecholamine-induced lipolysis in adipose tissue and skeletal muscle in obesity,” Physiology and Behavior, vol. 94, no. 2, pp. 219–230, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. A. C. P. Martins, H. E. Borges, R. M. G. Garcia, S. R. Carniatto, and P. C. F. Mathias, “Monosodium L-glutamate-induced obesity impaired the adrenal medullae activity,” Neuroscience Research Communications, vol. 28, no. 1, pp. 49–58, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Yoshida, H. Nishioka, and Y. Nakamura, “Reduced norepinephrine turnover in brown adipose tissue of pre-obese mice treated with monosodium-L-glutamate,” Life Sciences, vol. 36, no. 10, pp. 931–938, 1985. View at Publisher · View at Google Scholar · View at Scopus
  52. F. S. M. Leigh, L. N. Kaufman, and J. B. Young, “Diminished epinephrine excretion in genetically obese (ob/ob) mice and monosodium glutamate-treated rats,” International Journal of Obesity, vol. 16, no. 8, pp. 597–604, 1992. View at Google Scholar
  53. S. C. Kumer and K. E. Vrana, “Intricate regulation of tyrosine hydroxylase activity and gene expression,” Journal of Neurochemistry, vol. 67, no. 2, pp. 443–462, 1996. View at Google Scholar · View at Scopus
  54. L. Díaz-Flores, R. Gutiérrez, H. Varela, F. Valladares, H. Alvarez-Argüelles, and R. Borges, “Histogenesis and morphofunctional characteristics of chromaffin cells,” Acta Physiologica, vol. 192, no. 2, pp. 145–163, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. K. A. Albert, E. Helmer-Matyjek, and A. C. Nairn, “Calcium/phospholipid-depending protein kinase (protein kinase C) phosphorylates and activates tyrosine hydroxylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 24, pp. 7713–7717, 1984. View at Google Scholar
  56. A. Akaike, M. Sasa, Y. Tamura, H. Ujihara, and S. Takaori, “Effects of protein kinase C on the muscarinic excitation of rat adrenal chromaffin cells,” Japanese Journal of Pharmacology, vol. 61, no. 2, pp. 145–148, 1993. View at Google Scholar · View at Scopus
  57. G. M. Reaven, “The insulin resistance syndrome: definition and dietary approaches to treatment,” Annual Review of Nutrition, vol. 25, pp. 391–406, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. R. K. Campbell, “Fate of the beta-cell in the pathophysiology of type 2 diabetes,” Journal of the American Pharmacists Association, vol. 49, pp. S10–S15, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. S. P. Kalra and P. S. Kalra, “Neuroendocrine control of energy homeostasis: update on new insights,” Progress in brain research, vol. 181, pp. 17–33, 2010. View at Google Scholar · View at Scopus
  60. A. E. Hirata, I. S. Andrade, P. Vaskevicius, and M. S. Dolnikoff, “Monosodium glutamate (MSG)-obese rats develop glucose intolerance and insulin resistance to peripheral glucose uptake,” Brazilian Journal of Medical and Biological Research, vol. 30, no. 5, pp. 671–674, 1997. View at Google Scholar · View at Scopus
  61. L. Macho, M. Ficková, D. Ježová, and S. Zórad, “Late effects of postnatal administration of monosodium glutamate on insulin action in adult rats,” Physiological Research, vol. 49, no. 1, pp. S79–S85, 2000. View at Google Scholar · View at Scopus
  62. A. C. P. Thirone, J. B. C. Carvalheira, A. E. Hirata, L. A. Velloso, and M. J. A. Saad, “Regulation of Cbl-associated protein/Cbl pathway in muscle and adipose tissues of two animal models of insulin resistance,” Endocrinology, vol. 145, no. 1, pp. 281–293, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. S. L. Balbo, P. C. Mathias, M. L. Bonfleur et al., “Vagotomy reduces obesity in MSG-treated rats,” Research Communications in Molecular Pathology and Pharmacology, vol. 108, no. 5-6, pp. 291–296, 2000. View at Google Scholar · View at Scopus
  64. Y. W. Kim, J. Y. Kim, and S. K. Lee, “Surgical removal of visceral fat decreases plasma free fatty acid and increases insulin sensitivity on liver and peripheral tissue in monosodium glutamate (MSG)-obese rats,” Journal of Korean Medical Science, vol. 14, no. 5, pp. 539–545, 1999. View at Google Scholar · View at Scopus
  65. B. Jeanrenaud, “Neuro-endocrine disorders in obesity,” International Journal for Vitamin and Nutrition Research, vol. 29, pp. 41–48, 1986. View at Google Scholar · View at Scopus
  66. P. Mitrani, M. Srinivasan, C. Dodds, and M. S. Patel, “Autonomic involvement in the permanent metabolic programming of hyperinsulinemia in the high-carbohydrate rat model,” American Journal of Physiology, vol. 292, no. 5, pp. E1364–E1377, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. C. J. Nolan, J. L. Leahy, V. Delghingaro-Augusto et al., “Beta cell compensation for insulin resistance in Zucker fatty rats: increased lipolysis and fatty acid signalling,” Diabetologia, vol. 49, no. 9, pp. 2120–2130, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. E. G. Cawthorn and C. B. Chan, “Effect of pertussis toxin on islet insulin secretion in obese (fa/fa) Zucker rats,” Molecular and Cellular Endocrinology, vol. 75, no. 3, pp. 197–204, 1991. View at Publisher · View at Google Scholar · View at Scopus
  69. T. M. Tassava, T. Okuda, and D. R. Romsos, “Insulin secretion from ob/ob mouse pancreatic islets: effects of neurotransmitters,” American Journal of Physiology, vol. 262, no. 3, pp. E338–E343, 1992. View at Google Scholar · View at Scopus
  70. C. Cruciani-Guglielmacci, M. Vincent-Lamon, C. Rouch, M. Orosco, A. Ktorza, and C. Magnan, “Early changes in insulin secretion and action induced by high-fat diet are related to a decreased sympathetic tone,” American Journal of Physiology, vol. 288, no. 1, pp. E148–E154, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus