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Feast or Famine: The Sympathetic Nervous System Response to Nutrient Intake

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1. The use of tritiated norepinephrine (NE) to measure the turnover rate of NE in sympathetically innervated organs was pioneered in the laboratory of Julius Axelrod. This technique provides an organ specific assessment of sympathetic activity, integrated over a 24 h period, in free living laboratory animals. As such it has proved useful in estimating changes in sympathetic outflow in different physiologic and patho-physiologic states.

2. Studies employing NE turnover techniques in laboratory rodents have demonstrated conclusively that fasting suppresses and overfeeding stimulates the sympathetic nervous system (SNS). These changes in sympathetic activity also occur in humans.

3. Diet-induced changes in SNS activity are regulated by insulin-mediated glucose uptake and metabolism in central neurons sensitive to insulin and located anatomically in the ventro-medial hypothalamus. The regulation is imposed by descending inhibition of tonically active sympathetic brainstem centers.

4. Diet-induced changes in SNS activity mediate changes in energy production known as dietary thermogenesis. The capacity for dietary thermogenesis serves as a potential buffer against weight gain.

5. Insulin stimulated SNS activity contributes to obesity-related hypertension. The insulin resistance of obesity, and consequent hyperinsulinemia, drives sympathetically mediated thermogenesis, restoring energy balance at the expense of SNS over activity. The association of obesity and hypertension, therefore, may be the unintended consequence of mechanisms recruited in the obese to limit further weight gain.

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REFERENCES

  • Agata, J., Masuda, A., Takada, M., Higashiura, K., Murakami, H., Miyazaki, Y., and Shimamoto, K. (1997). High plasma immunoreactive leptin level in essential hypertension. Am. J. Hypertens. 10:1171–1174.

    Article  PubMed  CAS  Google Scholar 

  • Cassano, P. A., Segal, M. R., Vokonas, P. S., and Weiss, S. T. (1990). Body fat distribution, blood pressure, and hypertension: A prospective cohort study of men in the Normative Aging Study. Ann. Epidemiol. 1:33–48.

    Article  PubMed  CAS  Google Scholar 

  • Dulloo, A. G., Young, J. B., and Landsberg, L. (1988). Sympathetic nervous system responses to cold exposure and diet in rat skeletal muscle. Am. J. Physiol. 255:E180–E188.

    PubMed  CAS  Google Scholar 

  • Dunbar, J. X., Hu, Y., and Lu, H. (1997). Intracerebroventricular leptin increases lumbar and renal sympathetic nerve activity and blood pressure in normal rats. Diabetes 46:2040–2043.

    PubMed  CAS  Google Scholar 

  • Einhorn, D., Young, J. B., and Landsberg, L. (1982). Hypotensive effect of fasting: Possible involvement of the sympathetic nervous system and endogenous opiates. Science 217:727–729.

    Article  PubMed  CAS  Google Scholar 

  • Giacchetta, G., Faloia, E., Sardu, C., Camilloni, M. A., Mariniello, B., Gatti, C., Garrapa, G. G. M., Guerrieri, M., and Mantero, F. (2000). Gene expression of angiotensinogen in adipose tissue of obese patients. Int. J. Obes. 24(Suppl 2):S142–S143.

    Google Scholar 

  • Grassi, G., Seravalle, G., Cattaneo, B. M., Bolla, G. B., Lanfranchi, A., and Columbo, M. (1995). Sympathetic activation in obese normotensive subjects. Hypertension 25:560–563.

    PubMed  CAS  Google Scholar 

  • Grassi, G., Seravalle, G., Colombo, M., Bolla, G., Cattaneo, B. M., Cavagnini, F., and Mancia, G. (1998). Body weight reduction, sympathetic nerve traffic, and arterial baroreflex in obese normotensive humans. Circulation 97(20):2037–2042.

    PubMed  CAS  Google Scholar 

  • Grassi, G., Dell'Oro, R., Facchini, A., Trevano, F. Q., Bolla, G. B., and Mancia, G. (2004). Effect of central and peripheral body fat distribution on sympathetic an baroreflex function in obese normotensives J. Hypertens. 22:2363–2369.

    Article  PubMed  CAS  Google Scholar 

  • Hausberg, M., Mark, A. L., Hoffman, R. P., Sinkey, C. A., and Anderson, E. A. (1995). Dissociation of sympathoexcitatory and vasodilator actions of modestly elevated plasma insulin levels. J. Hypertens. 13:1015–1021.

    Article  PubMed  CAS  Google Scholar 

  • Haynes, W. G., Morgan, D. A., Walsh, S. A., Mark, A. L., and Sivitz, W. I. (1997). Receptor-mediated regional sympathetic nerve activation by leptin. J. Clin. Invest. 100:270–278.

    PubMed  CAS  Google Scholar 

  • Johnson, T. S., Young, J. B., and Landsberg, L. (1981). Norepinephrine turnover in lung: Effect of cold exposure and chronic hypoxia. J. Appl. Physiol. 51:614–620.

    PubMed  CAS  Google Scholar 

  • Johnson, T. S., Young, J. B., and Landsberg, L. (1983). Sympathoadrenal responses to acute and chronic hypoxia in the rat. J. Clin. Invest. 71:1263–1272.

    PubMed  CAS  Google Scholar 

  • Kaufman, L. N., Young, J. B., and Landsberg, L. (1986). Effect of protein on sympathetic nervous system activity in the rat: Evidence for nutrient-specific responses. J. Clin. Invest. 77:551–558.

    PubMed  CAS  Google Scholar 

  • Kissebah, A. H., Vydelingum, N., Murray, R., Evans, D. J., Hartz, A. J., Kalkhoff, R. K., and Adams, P. W. (1982). Relation of body fat distribution to metabolic complications of obesity. J. Clin. Endocrinol. Metab. 54:254–259.

    Article  PubMed  CAS  Google Scholar 

  • Landsberg, L. (1986). Diet, obesity and hypertension: an hypothesis involving insulin, the sympathetic nervous system, and adaptive thermogenesis. Q. J. Med. 236:1081–1090.

    Google Scholar 

  • Landsberg, L. (2004). Handbook of hypertension. In Birkenhäger, W. H., Robertson, J. I. S., and Zanchetti, A. (eds.), Hypertension in the Twentieth Century, Vol. 22, Elsevier BV, New York.

  • Landsberg, L., and Axelrod, J. (1968a). Reduced accumulation of 3-H-norepinephrine in the rat heart following hypophysectomy. Endocrinology 82:175–178.

    PubMed  CAS  Google Scholar 

  • Landsberg, L., and Axelrod, J. (1968b). Influence of pituitary, thyroid and adrenal hormones on norepinephrine turnover and metabolism in the rat heart. Circ. Res. 22:559–571.

    PubMed  CAS  Google Scholar 

  • Landsberg, L., and Axelrod, J. (1968c). The effect of elevated temperature on the retention of 3-H-norepinephrine in the hearts of normal and thyroidectomized rats. Life Sci. 7:1171–1175.

    Article  PubMed  CAS  Google Scholar 

  • Landsberg, L., and Young, J. B. (1978). Fasting feeding and the regulation of the sympathctic nervous system. N. Engl. J. Med. 298:1295–1301.

    Article  PubMed  CAS  Google Scholar 

  • Landsberg, L., and Young, J. B. (1985). Insulin-mediated glucose metabolism in the relationship between dietary intake and sympathetic nervous system activity. Int. J. Obesity 9(Suppl. 2):63–68.

    CAS  Google Scholar 

  • Landsberg, L., Greff, L., Gunn, S., and Young, J. B. (1980). Adrenergic mechanisms in the metabolic adaptation to fasting and feeding: Effects of phlorizin on diet-induced changes in sympathoadrenal activity in the rat. Metabolism 29:1128–1137.

    Article  PubMed  CAS  Google Scholar 

  • Landsberg, L., Saville, M. E., and Young, J. B. (1984). The sympathoadrenal system and regulation of thermogenesis. Am. J. Physiol. 247:E181–E189.

    PubMed  CAS  Google Scholar 

  • Larsson, B., Svardsudd, K., Welin, L., Wilhelmsen, L., Bjorntorp, P., and Tibblin, G. (1984). Abdominal adipose tissue distribution, obesity and risk of cardiovascular disease and death: 13 year follow up of participants in the study of men born in 1913. Br. Med. J. 288:1401–1404.

    Article  CAS  Google Scholar 

  • Neff, N. H., Tozer, T. N., Hammer, E., Costa, E., and Brodie, B. B. (1968). Application of steady-state kinetics to the uptake and decline of H3-NE in the rat heart. J. Pharmacol. Exp. Ther. 160:48–52.

    PubMed  CAS  Google Scholar 

  • O’Dea, K., Esler, M., Leondard, P., Stockigt, J. R., and Nestel, P. (1982). Noradrenaline turnover during under- and over-eating in normal weight subjects. Metabolism 31:896–899.

    Article  PubMed  CAS  Google Scholar 

  • O’Hare, J. A., Minaker, K. L., Meneilly, G. S., Rowe, J. W., Pallotta, J. A., and Young, J. B. (1989). Effect of insulin on plasma norepinephrine and 3,4-dihydroxyphenylalanine in obese men. Metabolism 38:322–329.

    Article  PubMed  CAS  Google Scholar 

  • Rappaport, E. B., Young, J. B., and Landsberg, L. (1982). Initiation, duration and dissipation of diet-induced changes in sympathetic nervous system activity in the rat. Metabolism 31:143–146.

    Article  PubMed  CAS  Google Scholar 

  • Rowe, J. W., Young, J. B., Minaker, K. L., Stevens, A. L., Pallotta, J., and Landsberg, L. (1981). Effect of insulin and glucose infusions on sympathetic nervous system activity in normal man. Diabetes 30:219–225.

    PubMed  CAS  Google Scholar 

  • Schwartz, J. H., Young, J. B., and Landsberg, L. (1983). Effect of dietary fat on sympathetic nervous system activity in the rat. J. Clin. Invest. 72:361–370.

    PubMed  CAS  Google Scholar 

  • Taubin, H. L., Djahanguiri, B., and Landsberg, L. (1972). Norepinephrine concentration and turnover in different regions of the gastrointestinal tract of the rat. An approach to the evaluation of sympatheticactivity in the gut. Gut 13:790–795.

    PubMed  CAS  Google Scholar 

  • Troisi, R. J., Weiss, S. T., Parker, D. R., Sparrow, D., Young, J. B., and Landsberg, L. (1991). Relation of obesity and diet to sympathetic nervous system activity. Hypertension 17:669–677.

    PubMed  CAS  Google Scholar 

  • Walgren, M. C., Young, J. B., Kaufman, L. N., and Landsberg, L. (1987). The effects of various carbohydrates on sympathetic activity in heart and interscapular brown adipose tissue (IBAT) of the rat. Metabolism 36(6):585–594.

    Article  PubMed  CAS  Google Scholar 

  • Young, J. B. (1988). Effect of experimental hyperinsulinemia on sympathetic nervous system activity in rat. Life Sci. 49:193–200.

    Article  Google Scholar 

  • Young, J. B., and Landsberg, L. (1977a). Suppression of sympathetic nervous system during fasting. Science 196:1473–1475.

    Article  PubMed  CAS  Google Scholar 

  • Young, J. B., and Landsberg, L. (1977b). Stimulation of the sympathetic nervous system during sucrose feeding. Nature 269:615–617.

    Article  PubMed  CAS  Google Scholar 

  • Young, J. B., and Landsberg, L. (1979a). Sympathoadrenal activity in fasting pregnant rats: Dissociation of adrenal medullary and sympathetic nervous system responses. J. Clin. Invest. 64:109–116.

    PubMed  CAS  Google Scholar 

  • Young, J. B., and Landsberg, L. (1979b). Effect of diet and cold exposure on norepinephrine turnover in pancreas and liver. Am. J. Physiol. 236:E524–E533.

    PubMed  CAS  Google Scholar 

  • Young, J. B., and Landsberg, L. (1980). Impaired suppression of sympathetic activity during fasting in the gold thioglucose-treated mouse. J. Clin. Invest. 65:1086–1094.

    PubMed  CAS  Google Scholar 

  • Young, J. B., Saville, E., Rothwell, N. J., Stock, M. J., and Landsberg, L. (1982). Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue in the rat. J. Clin. Invest. 69:1061–1071.

    Article  PubMed  CAS  Google Scholar 

  • Young, J. B., Fish, S., and Landsberg, L. (1983). Sympathetic nervous system and adrenal medullary response to ischemic injury in mice. Am. J. Physiol. 245:E67–E73.

    PubMed  CAS  Google Scholar 

  • Young, J. B., Rosa, R. M., and Landsberg, L. (1984). Dissociation of sympathetic nervous system and adrenal medullary responses. Am. J. Physiol. 247:E35–E40.

    PubMed  CAS  Google Scholar 

  • Young, J. B., Kaufman, L. N., Saville, M. E., and Landsberg, L. (1985). Increased sympathetic nervous system activity in rats fed a low protein diet: Evidence against a role for dietary tyrosine. Am. J. Physiol. 248:R627–R637.

    PubMed  CAS  Google Scholar 

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ACKNOWLEDGMENT

I remain profoundly grateful for Julie's mentorship, generosity, and for the infectious enthusiasm for science that he engendered in me, and many others, who were fortunate enough to work with him.

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  1. Northwestern University,Feinberg School of Medicine, Chicago, USA

    Lewis Landsberg

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Landsberg, L. Feast or Famine: The Sympathetic Nervous System Response to Nutrient Intake. Cell Mol Neurobiol 26, 495–506 (2006). https://doi.org/10.1007/s10571-006-9010-7

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