Hostname: page-component-745bb68f8f-d8cs5 Total loading time: 0 Render date: 2025-02-02T04:14:31.685Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain–adipose tissue cross talk

Published online by Cambridge University Press:  07 March 2007

Timothy J. Bartness ,
C. Kay Song ,
Haifei Shi ,
Robert R. Bowers  and
Michelle T. Foster
Timothy J. Bartness*
Affiliation:
Department of Biology, Neurobiology & Behavior Program Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30302–4010, USA
C. Kay Song
Affiliation:
Department of Biology, Neurobiology & Behavior Program Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30302–4010, USA
Haifei Shi
Affiliation:
Department of Biology, Neurobiology & Behavior Program Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30302–4010, USA
Robert R. Bowers
Affiliation:
Department of Biology, Neurobiology & Behavior Program Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30302–4010, USA
Michelle T. Foster
Affiliation:
Department of Biology, Neurobiology & Behavior Program Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA 30302–4010, USA
*
* Corresponding author: Dr Timothy J. Bartness, fax +1 404 651 2509, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

While investigating the reversible seasonal obesity of Siberian hamsters, direct sympathetic nervous system (SNS) postganglionic innervation of white adipose tissue (WAT) has been demonstrated using anterograde and retrograde tract tracers. The primary function of this innervation is lipid mobilization. The brain SNS outflow to WAT has been defined using the pseudorabies virus (PRV), a retrograde transneuronal tract tracer. These PRV-labelled SNS outflow neurons are extensively co-localized with melanocortin-4 receptor mRNA, which, combined with functional data, suggests their involvement in lipolysis. The SNS innervation of WAT also regulates fat cell number, as noradrenaline inhibits and WAT denervation stimulates fat cell proliferation in vitro and in vivo respectively. The sensory innervation of WAT has been demonstrated by retrograde tract tracing, electrophysiological recording and labelling of the sensory-associated neuropeptide calcitonin gene-related peptide in WAT. Local injections of the sensory nerve neurotoxin capsaicin into WAT selectively destroy this innervation. Just as surgical removal of WAT pads triggers compensatory increases in lipid accretion by non-excised WAT depots, capsaicin-induced sensory denervation triggers increases in lipid accretion of non-capsaicin-injected WAT depots, suggesting that these nerves convey information about body fat levels to the brain. Finally, parasympathetic nervous system innervation of WAT has been suggested, but the recent finding of no WAT immunoreactivity for the possible parasympathetic marker vesicular acetylcholine transporter (VAChT) argues against this claim. Collectively, these data suggest several roles for efferent and afferent neural innervation of WAT in body fat regulation.

Keywords

Sympathetic nervous systemSensory nervesParasympathetic nervous systemPseudorabies virusLipolysis
Type
Symposium on ‘Biology of obesity’
Information
Proceedings of the Nutrition Society , Volume 64 , Issue 1 , February 2005 , pp. 53 - 64
Copyright
Copyright © The Nutrition Society 2005

References

Aberdeen, J, Corr, L, Milner, P, Lincoln, J & Burnstock, G (1990) Marked increase in calcitonin gene-related peptide containing nerves in the developing rat following long-term sympathectomy with guanethidine. Neurosciences 35, 175–184.Google Scholar
Ainsworth, A, Halim, P, Wall, PD, Allt, G, Mackenzie, M, Gibson, S & Polak, J (1981) Effects of capsaicin applied locally to adult peripheral nerves. II. Anatomy and enzyme and peptide chemistry of peripheral nerve and spinal cord. Pain 11, 379–388.CrossRefGoogle ScholarPubMed
Ballantyne, B (1968) Histochemical and biochemical aspects of cholinesterase activity of adipose tissue. Archives Internationales de Pharmacodynamie et de Therapie 173, 343–350.Google Scholar
Ballantyne, B & Raftery, AT (1974) The intrinsic autonomic innervation of white adipose tissue. Cytobios 10, 187–197.Google Scholar
Ballard, K, Malmfors, T & Rosell, S (1974) Adrenergic innervation and vascular patterns in canine adipose tissue. Microvascular Research 8, 164–171.Google Scholar
Bamshad, M, Aoki, VT, Adkison, MG, Warren, WS & Bartness, TJ (1998) Central nervous system origins of the sympathetic nervous system outflow to white adipose tissue. American Journal of Physiology 275, R291–R299.Google ScholarPubMed
Bamshad, M, Song, CK & Bartness, TJ (1999) CNS origins of the sympathetic nervous system outflow to brown adipose tissue. American Journal of Physiology 276, R1569–R1578.Google Scholar
Bartness, TJ (1995) Short day-induced depletion of lipid stores is fat pad- and gender-specific in Siberian hamsters. Physiology and Behavior 58, 539–550.CrossRefGoogle ScholarPubMed
Bartness, TJ (1996) Photoperiod, sex, gonadal steroids and housing density affect body fat in hamsters. Physiology and Behavior 60, 517–529.CrossRefGoogle ScholarPubMed
Bartness, TJ (2002) Dual innervation of white adipose tissue: some evidence for parasympathetic nervous system involvement. Journal of Clinical Investigation 110, 1235–1237.CrossRefGoogle ScholarPubMed
Bartness, TJ & Bamshad, M (1998) Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. American Journal of Physiology 275, R1399–R1411.Google Scholar
Bartness, TJ, Demas, GE & Song, CK (2001) Central nervous system innervation of white adipose tissue. In Adipose Tissue, pp. 116–130 [Klaus, S, editors]. Georgetown, TX: Landes Bioscience.Google Scholar
Bartness, TJ, Demas, GE & Song, CK (2002) Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormones and the sympathetic nervous system. Experimental Biology and Medicine 227, 363–376.Google Scholar
Bartness, TJ & Fine, JB (1999) Melatonin and seasonal changes in body fat.In Melatonin in the Promotion of Health, 115–135 [Watson, RR, editors]. Boca Raton, FL: CRC.Google Scholar
Bartness, TJ & Goldman, BD (1988) Peak duration of serum melatonin and short day responses in adult Siberian hamsters. American Journal of Physiology 255, R812–R822.Google Scholar
Bartness, TJ & Goldman, BD (1989) Mammalian pineal melatonin: A clock for all seasons. Experientia 45, 939–945.Google Scholar
Bartness, TJ, Goldman, BD & Bittman, EL (1991) SCN lesions block responses to systemic melatonin infusions in Siberian hamsters. American Journal of Physiology 260, R102–R112.Google ScholarPubMed
Bartness, TJ, Hamilton, JM, Wade, GN & Goldman, BD (1989) Regional differences in fat pad responses to short days in Siberian hamsters. American Journal of Physiology 257, R1533–R1540.Google Scholar
Bartness, TJ & Wade, GN (1985) Photoperiodic control of seasonal body weight cycles in hamsters. Neuroscience and Behavioral Reviews 9, 599–612.Google Scholar
Bouloumie, A, Planat, V, Devedjian, JC, Valet, P, Saulnier-Blache, JS, Record, M & Lafontan, M (1994) Alpha 2-adrenergic stimulation promotes preadipocyte proliferation. Involvement of mitogen-activated protein kinases. Journal of Biological Chemistry 269, 30254–30259.Google Scholar
Bray, GA (1990) Obesity – a state of reduced sympathetic activity and normal or high adrenal activity (the autonomic and adrenal hypothesis revisited). International Journal of Obesity 14, 77–91.Google Scholar
Bray, GA (1991) Obesity, a disorder of nutrient partitioning: the MONA LISA hypothesis. Journal of Nutrition 121, 1146–1162.Google Scholar
Bray, GA & Nishizawa, Y (1978) Ventromedial hypothalamus modulates fat mobilisation during fasting. Nature 274, 900–901.Google Scholar
Butler, AA & Cone, RD (2002) The melanocortin receptors: lessons from knockout models. Neuropeptides 36, 77–84.Google Scholar
Cannon, WB (1939) The Wisdom of the Body, New York: Norton.CrossRefGoogle Scholar
Cantu, RC & Goodman, HM (1967) Effects of denervation and fasting on white adipose tissue. American Journal of Physiology 212, 207–212.Google Scholar
Card, JP, Rinaman, L, Schwaber, JS, Miselis, RR, Whealy, ME, Robbins, ME & Enquist, LW (1990) Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. Journal of Neuroscience 10, 1974–1994.Google Scholar
Castan, I, Valet, P, Larrouy, D, Voisin, T, Remaury, A, Daviaud, D, Laburthe, M & Lafontan, M (1993) Distribution of PYY receptors in human fat cells: an antilipolytic system alongside the alpha2-adrenergic system. American Journal of Physiology 265, E74–E80.Google Scholar
Castan, K, Valet, P, Quideau, N, Voisin, T, Ambid, L, Laburthe, M, Lafontan, M & Carpene, C (1994) Antilipolytic effects of alpha2-adrenergic agonists, neuropeptide Y, adenosine, and PGE1 in mammal adipocytes. American Journal of Physiology 266, R1141–R1147.Google Scholar
Clement, G (1950) La mobilisation des glycerides de reserve chez le rat. II. Influence due systeme nerveux sympathique. Etablissement d'un procede de mesure de I'intensite de la mobilisation (The mobilisation of glyceride reserves in the rat. II. Influence of the sympathetic nervous system. Establishing a process for measuring the intensity of the mobilisation). Archives de Sciences Physiologiques 4, 13–29.Google Scholar
Considine, RV, Considine, EL, Williams, CJ, Hyde, TM & Caro, JF (1996) The hypothalamic leptin receptor in humans: identification of incidental sequence polymorphisms and absence of the db/db mouse and fa/fa rat mutations. Diabetes 45, 992–994.Google Scholar
Cousin, B, Casteilla, L, Lafontan, M, Ambid, L, Langin, D, Berthault, M-F & Penicaud, L (1993) Local sympathetic denervation of white adipose tissue in rats induces preadipocyte proliferation without noticeable changes in metabolism. Endocrinology 133, 2255–2262.Google Scholar
Daniel, H & Derry, DM (1969) Criteria for differentiation of brown and white fat in the rat. Canadian Journal of Physiology and Pharmacology 47, 941–945.Google Scholar
Demas, GE & Bartness, TJ (2001a) Novel method for localized, functional sympathetic nervous system denervation of peripheral tissue using guanethidine. Journal of Neuroscience Methods 112, 21–28.CrossRefGoogle ScholarPubMed
Demas, GE & Bartness, TJ (2001b) Direct innervation of white fat and adrenal medullary catecholamines mediate photoperiodic changes in body fat. American Journal of Physiology 281, R1499–R1505.Google ScholarPubMed
Diculescu, I & Stoica, M (1970) Fluorescence histochemical investigations on the adrenergic innervation of the white adipose tissue in the rat. Journal of Neuro-visceral Relations 32, 25–36.Google Scholar
DiGirolamo, M, Fine, JB, Tagra, K & Rossmanith, R (1998) Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. American Journal of Physiology 274, R1460–R1467.Google ScholarPubMed
Dodt, C, Lonnroth, P, Wellhoner, JP, Fehm, HL & Elam, M (2003) Sympathetic control of white adipose tissue in lean and obese humans. Acta Physiologica Scandinavica 177, 351–357.Google Scholar
Dogiel, AS (1898) Die sensiblen Nervenendigungen im Herzen und in den Blutgefassen der Saugethiere (The afferent nerve endings in the heart and in the blood vessels of mammals). Archiv für Mikroskopischen Anatomie 52, 44–70.Google Scholar
Dua, A, Hennes, MI, Hoffmann, RG, Maas, DL, Krakower, GR, Sonnenberg, GE & Kissebah, AH (1996) Leptin: a significant indicator of total body fat but not of visceral fat and insulin insensitivity in African-American women. Diabetes 45, 1635–1637.Google Scholar
Dulloo, AG & Miller, DS (1987) Obesity: a disorder of the sympathetic nervous system. World Review of Nutrition and Dietetics 50, 1–56.Google Scholar
Edwards, SL, Anderson, CR, Southwell, BR & McAllen, RM (1996) Distinct preganglioinic neurons innervate noradrenaline and adrenaline cells in the cat adrenal medulla. Neurosciences 70, 825–832.Google Scholar
Enquist, LW & Card, JP (2003) Recent advances in the use of neurotropic viruses for circuit analysis. Current Opinion in Neurobiology 13, 603–606.Google Scholar
Faust, IM (1984) Role of the fat cell in energy balance physiology.In Eating and Its Disorders, 97–107 [Stunkard, AJ, Stellar, E, editors]. New York: Raven Press.Google Scholar
Ferry, G, Tellier, E, Try, A, Gres, S, Naime, I, Simon, MF et al. (2003) Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation. Up-regulated expression with adipocyte differentiation and obesity. Journal of Biological Chemistry 278, 18162–18169.Google Scholar
Fishman, RB & Dark, J (1987) Sensory innervation of white adipose tissue. American Journal of Physiology 253, R942–R944.Google Scholar
Frederich, RC, Lollmann, B, Hamann, A, Napolitano-Rosen, A, Kahn, BB, Lowell, BB & Flier, JS (1995) Expression of ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. Journal of Clinical Investigation 96, 1658–1663.Google Scholar
Fredholm, BB (1985) Nervous control of circulation and metabolism in white adipose tissue.In New Perspectives in Adipose Tissue: Structure, Function and Development, 45–64 [Cryer, A Van, RLR, editors]. Boston, MA: Butterworth.Google Scholar
Garofalo, MAR, Kettelhut, IC, Roselino, JES & Migliorini, RH (1996) Effect of acute cold exposure on norepinephrine turnover rates in rat white adipose tissue. Journal of the Autonomic Nervous System 60, 206–208.Google Scholar
Gasteyger, C & Tremblay, A (2002) Metabolic impact of body fat distribution. Journal of Endocrinological Investigation 25, 876–883.Google Scholar
Giordano, A, Morroni, M, Santone, G, Marchesi, GF & Cinti, S (1996) Tyrosine hydroxylase, neuropeptide Y, substance P, calcitonin gene-related peptide and vasoactive intestinal peptide in nerves of rat periovarian adipose tissue: an immunohistochemical and ultrastructural investigation. Journal of Neurocytology 25, 125–136.CrossRefGoogle ScholarPubMed
Gold, RM (1973) Hypothalamic obesity: the myth of the ventromedial nucleus. Science 182, 488–490.CrossRefGoogle ScholarPubMed
Gold, RM, Jones, AP & Sawchenko, PE (1977) Paraventricular area: critical focus of a longitudinal neurocircuitry mediating food intake. Physiology and Behavior 18, 1111–1119.Google Scholar
Gwyn, DG, Ritchie, TC & Coulter, JD (1985) The central distribution of vagal catecholaminergic neurons which project into the abdomen in the rat. Brain Research 328, 139–144.Google Scholar
Hardie, LJ, Rayner, DV, Holmes, S & Trayhurn, P (1996) Circulating leptin levels are modulated by fasting, cold exposure and insulin administration in lean but not Zucker (fa/fa) rats as measured by ELISA. Biochemical and Biophysical Research Communications 223, 660–665.Google Scholar
Harris, RBS (2000) Leptin – much more than a satiety signal. Annual Review of Nutrition 20, 45–75.Google Scholar
Haskell-Luevano, C, Miwa, H, Dickinson, C, Hruby, VJ, Yamada, T & Gantz, I (1994) Binding and cAMP studies of melanotropin peptides with the cloned human peripheral melanocortin receptor, hMC1R. Biochemical and Biophysical Research Communications 204, 1137–1142.Google Scholar
Hausman, DB, DiGirolamo, M, Bartness, TJ, Hausman, GJ & Martin, RJ (2001) The biology of white adipocyte proliferation. Obesity Reviews 2, 239–254.Google Scholar
Hill, B, Ralevic, V, Crowe, R & Burnstock, G (1996) Innervation and nitric oxide modulation of mesenteric arteries of the Golden hamster. European Journal of Pharmacology 317, 275–283.Google Scholar
Hillarp, NA & Hokfelt, B (1953) Evidence of adrenaline and noradrenaline in separate adrenal medullary cells. Acta Physiologica Scandinavica 30, 55–68.Google Scholar
Hoffman, GE, Smith, MS & Verbalis, JG (1993) c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Frontiers in Neuroendocrinology 14, 173–213.Google Scholar
Hwa, JJ, Ghibaudi, L, Gao, J & Parker, EM (2001) Central melanocortin system modulates energy intake and expenditure of obese and lean Zucker rats. American Journal of Physiology 281, R444–R451.Google Scholar
Jansco, G, Kiraly, E, Jansco-Gabor, A (1980) Direct evidence for an axonal site of action of capsaicin. Naunyn Schmiedeburgs Archives of Pharmacology 31, 91–94.Google Scholar
Janssen, I, Fortier, A, Hudson, R & Ross, R (2002) Effects of an energy-restrictive diet with or without exercise on abdominal fat, intermuscular fat, and metabolic risk factors in obese women. Diabetes Care 25, 431–438.Google Scholar
Jones, DD, Ramsay, TG, Hausman, GJ & Martin, RJ (1992) Norepinephrine inhibits rat pre-adipocyte proliferation. International Journal of Obesity 16, 349–354.Google Scholar
Kalia, M, Fuxe, K, Goldstein, M, Harfstrand, A, Agnati, LF & Coyle, JT (1984) Evidence for the existence of putative dopamine-, adrenaline- and noradrenaline-containing vagal motor neurons in the brainstem of the rat. Neuroscience Letters 50, 57–62.Google Scholar
Kirtland, J & Gurr, MI (1979) Adipose tissue cellularity: a review 2. The relationship between cellularity and obesity. International Journal of Obesity 3, 15–55.Google Scholar
Kras, KM, Hausman, DB, Hausman, GJ & Martin, RJ (1999) Adipocyte development is dependent upon stem cell recruitment and proliferation of preadipocytes. Obesity Research 7, 491–497.Google Scholar
Kreier, F, Fliers, E, Voshol, PJ, Van Eden, CG, Havekes, LM, Kalsbeek, A, Van Heijningen, CL, Sluiter, AA, Mettenleiter, TC, Romijn, JA, Sauerwein, HP & Buijs, RM (2002) Selective parasympathetic innervation of subcutaneous and intra-abdominal fat – functional implications. Journal of Clinical Investigation 110, 1243–1250.Google Scholar
Lafontan, M & Berlan, M (1993) Fat cell adrenergic receptors and the control of white and brown fat cell function. Journal of Lipid Research 34, 1057–1091.CrossRefGoogle ScholarPubMed
Lazzarini, SJ & Wade, GN (1991) Role of sympathetic nerves in effects of estradiol on rat white adipose tissue. American Journal of Physiology 260, R47–R51.Google Scholar
Luiten, PGM, ter, Horst, GJ, Karst, H, Steffens AB (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Research 329, 374–378.Google Scholar
Maffei, M, Fei, H, Lee, GH, Dani, C, Leroy, P, Zhang, Y, Proenca, R, Negrel, R, Ailhaud, G & Friedman, JM (1995) Increased expression in adipocytes of ob RNA in mice with lesions of the hypothalamus and with mutations at the db locus. Proceedings of the National Academy of Sciences USA 92, 6957–6960.Google Scholar
Mantzoros, CS, Qu, DQ, Frederich, RC, Susulic, VS, Lowell, BB, Maratos-Flier, E & Flier, JS (1996) Activation of β 3 adrenergic receptors suppresses leptin expression and mediates a leptin-independent inhibition of food intake in mice. Diabetes 45, 909–914.Google Scholar
Mauer, MM & Bartness, TJ (1996) Photoperiod-dependent fat pad mass and cellularity changes following partial lipectomy in Siberian hamsters. American Journal of Physiology 270, R383–R392.Google Scholar
Migliorini, RH, Garofalo, MAR & Kettelhut, IC (1997) Increased sympathetic activity in rat white adipose tissue during prolonged fasting. American Journal of Physiology 272, R656–R661.Google Scholar
Mione, M, Cavanagh, JFR, Kirkpatrick, KA & Burnstock, G (1992) Plasticity in expression of calcitonin gene-related peptide and substance P immunoreactivity in ganglia and fibres following guanethidine and/or capsaicin denervation. Cell Tissue Research 268, 491–504.Google Scholar
Morrison, SF (2001) Differential control of sympathetic outflow. American Journal of Physiology 281, R683–R698.Google Scholar
Newsholme, EA & Leech, AR (1983) Biochemistry for the Medical Sciences, Chichester West Sussex: John Wiley.Google Scholar
Ng, TB & Wong, CM (1986) Effects of pineal indoles and arginine vasotocin on lipolysis and lipogenesis in isolated adipocytes. Journal of Pineal Research 3, 55–66.Google Scholar
Niijima, A (1998) Afferent signals from leptin sensors in the white adipose tissue of the epididymis, and their reflex effect in the rat. Journal of the Autonomic Nervous System 73, 19–25.Google Scholar
Nishizawa, Y & Bray, GA (1978) Ventromedial hypothalamic lesions and the mobilization of fatty acids. Journal of Clinical Investigation 61, 714–721.Google Scholar
Ollmann, MM, Wilson, BD, Yang, YK, Kerns, JA, Chen, Y, Gantz, I & Barsh, GS (1997) Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278, 135–138.CrossRefGoogle ScholarPubMed
Orban, Z, Remaley, AT, Sampson, M, Trajanoski, Z & Chrousos, GP (1999) The differential effect of food intake and beta-adrenergic stimulation on adipose-derived hormones and cytokines in man. Journal of Clinical Endocrinology and Metabolism 84, 2126–2133.Google Scholar
Ostlund, RE, Jr, Yang, JW, Klein, S, Gingerich R (1996) Relation between plasma leptin concentration and body fat, gender, diet, age, and metabolic covariates. Journal of Clinical Endocrinology and Metabolism 81, 3909–3913.Google Scholar
Ozaki, N, Sugiura, Y, Yamamoto, M & Nishiyama, Y (1996) Induction of Fos protein expression in spinal cord neurons by herpes simplex virus infections in the mouse. Neuroscience Letters 216, 61–64.Google Scholar
Pasanisi, F, Contaldo, F, de Simone, G & Mancini, M (2001) Benefits of sustained moderate weight loss in obesity. Nutrition Metabolism and Cardiovascular Diseases 11, 401–406.Google Scholar
Powley, TL, Walgren, MC & Laughton, WB (1983) Effects of guanethidine sympathectomy on ventromedial hypothalamic obesity. American Journal of Physiology 245, R408–R420.Google Scholar
Ralevic, V, Karoon, P & Burnstock, G (1995) Long-term sensory denervation by neonatal capsaicin treatment augments sympathetic neurotransmission in rat mesenteric arteries by increasing levels of norepinephrine and selectively enhancing postjunctional actions. Journal of Pharmacology and Experimental Therapeutics 274, 64–71.Google Scholar
Raposinho, PD, White, RB & Aubert, ML (2003) The melanocortin agonist melanotan-II reduces the orexigenic and adipogenic effects of neuropeptide Y (NPY) but does not affect the NPY-driven suppressive effects on the gonadotropic and somatotropic axes in the male rat. Journal of Neuroendocrinology 15, 173–181.Google Scholar
Rayner, DV, Simon, E, Duncan, JS & Trayhurn, P (1998) Hyperleptinaemia in mice induced by administration of the tyrosine hydroxylase inhibitor alpha-methyl-p-tyrosine. FEBS Letters 429, 395–398.Google Scholar
Rebuffe-Scrive, M (1991) Neuroregulation of adipose tissue: molecular and hormonal mechanisms. International Journal of Obesity 15, 83–86.Google Scholar
Rizack, MA (1961) An epinephrine-sensitive lipolytic activity in adipose tissue. Journal of Biological Chemistry 236, 657–662.Google Scholar
Robidoux, J, Pirouzi, P, Lafond, J & Savard, R (1995) Site-specific effects of sympathectomy on the adrenergic control of lipolysis in hamster fat cells. Canadian Journal of Physiology and Pharmacology 73, 450–458.Google Scholar
Rubino, A, Ralevic, V & Burnstock, G (1997) Sympathetic neurotransmission in isolated rat atria after sensory-motor denervation by neonatal treatment with capsaicin. Journal of Pharmacology and Experimental Therapeutics 282, 671–675.Google Scholar
Schafer, MK, Eiden, LE & Weihe, E (1998) Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. II. The peripheral nervous system. Neuroscience 84, 361–376.Google Scholar
Shi, H & Bartness, TJ (2001) Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Research Bulletin 54, 375–385.Google Scholar
Shi, H, Giordano, A, Cinti, S & Bartness, TJ (2005) Sensory or sympathetic white adipose tissue denervation differentially affects depot growth and cellularity American Journal of Physiology.Google Scholar
Sivitz, WI, Fink, BD, Morgan, DA, Fox, JM, Donohoue, PA & Haynes, WG (1999) Sympathetic inhibition, leptin, and uncoupling protein subtype expression in normal and fasting rats. American Journal of Physiology 277, E668–E677.Google Scholar
Skofitsch, G & Jacobowitz, DM (1985) Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 6, 747–754.Google Scholar
Slavin, BG & Ballard, KW (1978) Morphological studies on the adrenergic innervation of white adipose tissue. Anatomical Record 191, 377–389.Google Scholar
Song, CK & Bartness, TJ (1996) The effects of anterior hypothalamic lesions on short-day responses in Siberian hamsters given timed melatonin infusions. Journal of Biological Rhythms 11, 14–26.Google Scholar
Song, CK & Bartness, TJ (1998) Dorsocaudal SCN microknife-cuts do not block short day responses in Siberian hamsters given melatonin infusions. Brain Research Bulletin 45, 239–246.Google Scholar
Song, CK & Bartness, TJ (2001) CNS sympathetic outflow neurons to white fat that express melatonin receptors may mediate seasonal adiposity. American Journal of Physiology 281, R666–R672.Google Scholar
Strack, AM & Loewy, AD (1990) Pseudorabies virus: a highly specific transneuronal cell body marker in the sympathetic nervous system. Journal of Neuroscience 10, 2139–2147.Google Scholar
Strack, AM, Sawyer, WB, Platt, KB & Loewy, AD (1989) CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Research 491, 274–296.Google Scholar
Sved, AF, Cano, G & Card, JP (2001) Neuroanatomical specificity of the circuits controlling sympathetic outflow to different targets. Clinical and Experimental Pharmacology and Physiology 28, 115–119.Google Scholar
Takahashi, A, Ikarashi, Y, Ishimaru, H & Maruyama, Y (1993) Compensation between sympathetic nerves and adrenal medullary activity: effects of adrenomedullation and chemical sympathectomy on catecholamine turnover. Life Sciences 53, 1567–1572.CrossRefGoogle ScholarPubMed
Takahashi, A & Shimazu, T (1981) Hypothalamic regulation of lipid metabolism in the rat: effect of hypothalamic stimulation on lipolysis. Journal of the Autonomic Nervous System 4, 195–205.Google Scholar
Trayhurn, P, Duncan, JS, Hoggard, N & Rayner, DV (1998) Regulation of leptin production: a dominant role for the sympathetic nervous system. Proceedings of the Nutrition Society 57, 413–419.CrossRefGoogle ScholarPubMed
Trayhurn, P, Duncan, JS & Rayner, DV (1995) Acute cold-induced suppression of ob (obese) gene expression in white adipose tissue of mice: mediation by the sympathetic nervous system. Biochemical Journal 311, 729–733.Google Scholar
Trayhurn, P, Duncan, JS, Rayner, DV & Hardie, LJ (1996) Rapid inhibition of ob gene expression and circulating leptin levels in lean mice by the beta 3-adrenoceptor agonists BRL 35135A and ZD2079. Biochemical and Biophysical Research Communications 228, 605–610.Google Scholar
Turek, FW & Campbell, CS (1979) Photoperiodic regulation of neuroendocrine-gonadal activity. Biology of Reproduction 20, 32–50.Google Scholar
Turtzo, LC, Marx, R & Lane, MD (2001) Cross-talk between sympathetic neurons and adipocytes in coculture. Proceedings of the National Academy of Sciences USA 98, 12385–12390.Google Scholar
Underwood, H & Goldman, BD (1987) Vertebrate circadian and photoperiodic systems: role of the pineal gland and melatonin. Journal of Biological Rhythms 2, 279–315.Google Scholar
Vague, J, Vague, P, Tramoni, M, Vialettes, B & Mercier, P (1980) Obesity and diabetes. Acta Diabetologica Latina 17, 87–99.Google Scholar
Valet, P, Pages, C, Jeanneton, O, Daviaud, D, Barbe, P, Record, M, Saulnier-Blache, JS & Lafontan, M (1998) Alpha 2-adrenergic receptor-mediated release of lysophosphatidic acid by adipocytes. A paracrine signal for preadipocyte growth. Journal of Clinical Investigation 101, 1431–1438.Google Scholar
Wade, GN & Bartness, TJ (1984) Effects of photoperiod and gonadectomy on food intake, body weight and body composition in Siberian hamsters. American Journal of Physiology 246, R26–R30.Google Scholar
Weiss, ML & Chowdhury, SI (1998) The renal afferent pathways in the rat: a pseudorabies virus study. Brain Research 812, 227–241.Google Scholar
White, JE & Engel, FL (1958) A lipolytic action of epinephrine and norepinephrine on rat adipose tissue in vitro. Proceedings of the Society for Experimental Biology and Medicine 99, 375–378.Google Scholar
Wirsen, C (1964) Adrenergic innervation of adipose tissue examined by fluorescence microscopy. Nature 202, 913.Google Scholar
Wright, JT & Hausman, GJ (1990) Monoclonal antibodies against cell surface antigens expressed during porcine adipocyte differentiation. International Journal of Obesity 14, 284–291.Google Scholar
Young, JB, Saville, E, Rothwell, NJ, Stock, MJ & Landsberg, L (1982) Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. Journal of Clinical Investigation 69, 1061–1071.Google Scholar
Youngstrom, TG & Bartness, TJ (1995) Catecholaminergic innervation of white adipose tissue in the Siberian hamster. American Journal of Physiology 268, R744–R751.Google Scholar
Youngstrom, TG & Bartness, TJ (1998) White adipose tissue sympathetic nervous system denervation increases fat pad mass and fat cell number. American Journal of Physiology 275, R1488–R1493.Google Scholar
Zhang, Y, Proenca, R, Maffei, M, Barone, M, Leopold, L & Friedman, JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.Google Scholar