Sympathetic and sensory innervation of brown adipose tissue

International Journal of Obesity

Volumn 34, Issue , 2010, Pages S36-S42

  Bartness, T J ^a   Vaughan, C H ^a   Song, C K ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Brown fat; Sensory nerves; Sympathetic nervous system; Thermogenesis; Ucp 1

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PERILIPIN; UNCOUPLING PROTEIN 1;

BROWN ADIPOSE TISSUE; CATECHOLAMINE NERVE CELL; CHOLINERGIC SYSTEM; COLD EXPOSURE; CONFERENCE PAPER; ENERGY EXPENDITURE; HUMAN; IMMUNOREACTIVITY; LIPOLYSIS; NEUROCHEMISTRY; NONHUMAN; NUTRITIONAL STATUS; OBESITY; PHOTOPERIODICITY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; SENSORY NERVE CELL; SYMPATHETIC INNERVATION; WEIGHT GAIN;

ADIPOSE TISSUE, BROWN; ANIMALS; HUMANS; ION CHANNELS; MITOCHONDRIAL PROTEINS; SYMPATHETIC NERVOUS SYSTEM; THERMOGENESIS;

SUID HERPESVIRUS 1;

EID: 78449285575     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2010.182     Document Type: Article

References (86)

1. Gesner C. Medici Tigurini Historiae Animalium Liber I de Quadrupedibusuiuiparis. Froschauer, 1551, pp 840–844.
2. Sheldon EF. The so-called hibernating gland in mammals: A form of adipose tissue. Anat Rec 1924; 28: 331–347.
3. Smalley RL, Dryer RL. Brown fat: Thermogenic effect during arousal from hibernation in the bat. Science 1963; 140: 1333–1334.
4. Smith RE, Hock RJ. Brown fat: Thermogenic effector of arousal in hibernators. Science 1963; 140: 199–200.
5. Hayward JS, Lyman CP, Taylor CR. The possible role of brown fat as a source of heat during arousal from hibernation. Ann N YAcad Sci 1965; 131: 441–446.
6. Griggio MA. Thermogenic mechanisms in cold-acclimated animals. Braz J Med Biol Res 1988; 21: 171–176.
7. Heldmaier G, Klaus S, Wiesinger H, Friedrichs U, Wenzel M. Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds). Living in the Cold II. John Libbey Eurotext: Montrouge, France, 1989, pp 347–358.
8. Sell H, Deshaies Y, Richard D. The brown adipocyte: Update on its metabolic role. Int J Biochem Cell Biol 2004; 36: 2098–2104.
9. Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature 1979; 281: 31–35.
10. Cannon B, Houstek J, Nedergaard J. Brown adipose tissue. More than an effector of thermogenesis? Ann N Y Acad Sci 1998; 856: 171–187.
11. Nakamura K, Matsumura K, Kobayashi S, Kaneko T. Sympathetic premotor neurons mediating thermoregulatory functions. Neurosci Res 2005; 51: 1–8.
12. Rousset S, ves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, The biology of mitochondrial uncoupling proteins. Diabetes 2004; 53 (1): S130–S135.
13. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2007; 293: E444–E452.
14. Cannon B, Nedergaard J. Brown adipose tissue: Function and physiological significance. Physiol Rev 2004; 84: 277–359.
15. Giordano A, Frontini A, Castellucci M, Cinti S. Presence and distribution of cholinergic nerves in rat mediastinal brown adipose tissue. J Histochem Cytochem 2004; 52: 923–930.
16. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009; 360: 1509–1517.
17. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 2009; 58: 1526–1531.
18. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518–1525.
19. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 1500–1508.
20. Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J 2009; 23: 3113–3120.
21. Wirsen C. Adrenergic innervation of adipose tissue examined by fluorescence microscopy. Nature 1964; 202: 913.
22. Wirsen C. Distribution of adrenergic nerve fibers in brown and white adipose tissue. In: Renold AE, Cahill GFJ (eds). Adipose Tissue. Am. Physiol. Soc.: Washington, DC, 1965, pp 197–199.
23. Bargmann W, Hehn GV, Linder E. ber die Zellen des braunen Fettgewebes und ihre Innervation. Z Zellforsch Mikroskop Anat 1968; 85: 601–613.
24. Himms-Hagen J. Neural control of brown adipose tissue thermogenesis, hypertrophy, and atrophy. Front Neuroendocinol 1991; 12: 38–93.
25. Bartness TJ, Song CK, Demas GE. Central nervous system innervation of brown adipose tissue. In: Klaus S (ed). Adipose Tissue. Landes Bioscience: Georgetown, TX, 2001, pp 162–200.
26. Bartness TJ, Song CK. Innervation of brown adipose tissue and its role in thermogenesis. Can J Diabetes 2005; 29: 420–428.
27. Trayhurn P, Milner RE. A commentary on the interpretation of in vitro biochemical measures of brown adipose tissue thermogenesis. Can J Physiol Pharmacol 1989; 67: 811–819.
28. Bamshad M, Song CK, Bartness TJ. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am J Physiol 1999; 276: R1569–R1578.
29. Oldfield BJ, Giles ME, Watson A, Anderson C, Colvill LM, McKinley MJ. The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat. Neuroscience 2002; 110: 515–526.
30. Cao WH, Fan W, Morrison SF. Medullary pathways mediating specific sympathetic responses to activation of dorsomedial hypothalamus. Neuroscience 2004; 126: 229–240.
31. Song CK, Vaughan CH, Keen-Rhinehart E, Harris RB, Richard D, Bartness TJ. Melanocortin-4 receptor mRNA expressed in sympathetic outflow neurons to brown adipose tissue: Neuroanatomical and functional evidence. Am J Physiol 2008; 295: R417–R428.
32. Leitner C, Bartness TJ. Acute brown adipose tissue temperature response to cold in monosodium glutamate-treated Siberian hamsters. Brain Res 2009; 1292: 38–51.
33. Bartness TJ. Viral labeling of the CNS origins of the sympathetic nervous system innervation of brown adipose tissue: Implications for torpor and hibernation responses. In: Heldmaier G, Klaus S, Klingenspor M (eds). Life in the Cold. Springer-Verlag: Berlin, 2004, pp 401–411.
34. 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 1998; 275: R291–R299.
35. Song CK, Bartness TJ. CNS sympathetic outflow neurons to white fat that express melatonin receptors may mediate seasonal adiposity. Am J Physiol 2001; 281: R666–R672.
36. Foster DO, Depocas F, Zuker M. Heterogeneity of the sympathetic innervation of rat interscapular brown adipose tissue via intercostal nerves. Can J Physiol Pharmacol 1982; 60: 747–754.
37. Foster DO, Depocas F, Zaror-Behrens G. Unilaterality of the sympathetic innervation of each pad of interscapular brown adipose tissue. Can J Physiol 1982; 60: 107–113.
38. Wantanabe J, Mishiro K, Amatsu T, Kanamura S. Absence of paravascular nerve projection and cross-innervation in interscapular brown adipose tissue of mice. J Auton Nerv Syst 1994; 49: 269–276.
39. Desautels M, Dulos RA. Role of neural input in photoperiodinduced changes in hamster brown adipose tissue. Can J Physiol Pharmacol 1990; 68: 677–681.
40. Hamilton JM, Bartness TJ, Wade GN. Effects of norepinephrine and denervation on brown adipose tissue in Syrian hamsters. Am J Physiol 1989; 257: R396–R404.
41. Meywirth A, Redlin U, Steinlechner S, Heldmaier G, Reiter RJ. Role of the sympathetic innervation in the cold-induced activation of 50-deiodinase in brown adipose tissue of the Djungarian hamster. Can J Physiol Pharmacol 1990; 69: 1896–1900.
42. Seydoux J, Constantinidis H, Tsacopoulos H, Girardier L. In vitro study of the control of the metabolic activity of brown adipose tissue by the sympathetic nervous system. J Physiol (Paris) 1977; 73: 985–996.
43. Girardier L, Seydoux J. Neural control of brown adipose tissue. In: Trayhurn P, Nicholls DG (eds). Brown Adipose Tissue. Edward Arnold: London, 1986, pp 122–151.
44. Silva JE, Larsen PR. Adrenergic activation of triiodothyronine production in brown adipose tissue. Nature 1983; 305: 712–713.
45. Takahashi A, Shimazu T, Maruyama Y. Importance of sympathetic nerves for the stimulatory effect of cold exposure on glucose utilization in brown adipose tissue. Jpn J Physiol 1992; 42: 653–664.
46. Rothwell NJ, Stock MJ. Effects of denervating brown adipose tissue on the responses to cold, hyperphagia and noradrenaline treatment in the rat. J Physiol 1984; 355: 457–463.
47. Benzi RH, Shibata M, Seydoux J, Girardier L. Prepontine knife cutinduced hyperthermia in the rat. Effect of chemical sympathectomy and surgical denervation of brown adipose tissue. Pflugers Arch 1988; 411: 593–599.
48. Rothwell NJ. Central effects of TNF alpha on thermogenesis and fever in the rat. Biosci Rep 1988; 8: 345–352.
49. Bryant KR, Rothwell NJ, Stock MJ, Wyllie MG. Parasympathethic effects on diet-induced thermogenesis. Eur J Pharmacol 1983; 95: 291–294.
50. Andrews PL, Rothwell NJ, Stock MJ. Effects of subdiaphragmatic vagotomy on energy balance and thermogenesis in the rat. J Physiol 1985; 362: 1–12.
51. Andrews PLR, Rothwell NJ, Stock MJ. Influence of subdiaphragmatic vagotomy and brown fat sympathectomy on thermogenesis in rats. Am J Physiol 1985; 249: E239–E243.
52. Schafer MK, Eiden LE, Weihe E. Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. II. The peripheral nervous system. Neuroscience 1998; 84: 361–376.
53. Song CK, Enquist LW, Bartness TJ. New developments in viral tracings of neural circuits. Virus Res 2005; 11: 235–249.
54. Raposinho PD, White RB, Aubert ML. 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. J Neuroendocrinol 2003; 15: 173–181.
55. Brito MN, Brito NA, Baro DJ, Song CK, Bartness TJ. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 2007; 148: 5339–53347.
56. Song CK, Jackson RM, Harris RB, 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 2005; 289: R1467–R1476.
57. Shrestha YB, Vaughan CH, Smith BJ, Song CK, Baro DJ, Bartness TJ. Central melanocortin stimulation increases phosphorylated perilipin A and hormone sensitive lipase in adipose tissues. Am J Physiol 2010; 299: R140–R149.
58. Williams DL, Bowers RR, Bartness TJ, Kaplan JM, Grill HJ. Brainstem melanocortin 3/4 receptor stimulation increases uncoupling protein gene expression in brown fat. Endocrinology 2003; 144: 4692–4697.
59. Grill HJ. Distributed neural control of energy balance: Contributions from hindbrain and hypothalamus. Obesity (Silver Spring) 2006; 14 (5): 216S–221S.
60. Grill HJ, Norgren R. The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res 1978; 143: 281–297.
61. Grill HJ, Norgren R. Neurological tests and behavioral deficits in chronic thalamic and chronic decerebrate rats. Brain Res 1978; 143: 299–312.
62. Nautiyal KM, Dailey MJ, Brito NA, Brito MN, Harris RBS, Bartness TJ, Energetic responses to cold temperatures in rats lacking forebrain-caudal brainstem connections. Am J Physiol 2008; 295: R789–R798.
63. Morrison SF, Nakamura K, Madden CJ. Central control of thermogenesis in mammals. Exp Physiol 2008; 93: 773–797.
64. Rathner JA, Owens NC, McAllen RM. Cold-activated raphe-spinal neurons in rats. J Physiol 2001; 535 (Part 3): 841–854.
65. Uno T, Roth J, Shibata M. Influence of the hypothalamus on the midbrain tonic inhibitory mechanism on metabolic heat production in rats. Brain Res Bull 2003; 61: 129–138.
66. Grill HJ, Kaplan J, Kaplan JM. Caudal brainstem participates in the distributed neural control of feeding. In: Stricker EM (ed). Neurobiology of Food and Fluid Intake. Plenum Press: New York, 1990, pp 125–149.
67. Norman D, Mukherjee S, Symons D, Jung RT, Lever JD. Neuropeptides in interscapular and perirenal brown adipose tissue in the rat: A plurality of innervation. J Neurocytol 1988; 17: 305–311.
68. Giordano A, Morroni M, Santone G, Marchesi GF, Cinti S. 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. J Neurocytol 1996; 25: 125–136.
69. Lever JD, Mukherjee S, Norman D, Symons D, Jung RT. Neuropeptide and noradrenaline distributions in rat interscapular brown fat and in its intact and obstructed nerves of supply. J Auton Nerv Syst 1988; 25: 15–25.
70. Ainsworth A, Halim P, Wall PD, Allt G, Mackenzie M, Gibson S, Effects of capsaicin applied locally to adult peripheral nerves. II Anatomy and enzyme and peptide chemistry of peripheral nerve and spinal cord. Pain 1981; 11: 379–388.
71. Cui J, Himms-Hagen J. Long-term decrease in body fat and in brown adipose tissue in capsaicin-desensitized rats. Am J Physiol 1992; 262: R568–R573.
72. Himms-Hagen J, Cui J, Sigurdson SL. Sympathetic and sensory nerves in control of growth of brown adipose tissue: effects of denervation and of capsaicin. Neurochem Int 1990; 17: 271–279.
73. Shi H, Song CK, Giordano A, Cinti S, Bartness TJ. Sensory or sympathetic white adipose tissue denervation differentially affects depot growth and cellularity. Am J Physiol 2005; 288: R1028–R1037.
74. Shi H, Bartness TJ. White adipose tissue sensory nerve denervation mimics lipectomy-induced compensatory increases in adiposity. Am J Physiol 2005; 289: R514–R520.
75. Dix RD, McKendall RR, Baringer JR. Comparative neurovirulence of herpes simplex virus type 1 strains after peripheral or intracerebral inoculation of BALB/c mice. Infect Immun 1983; 40: 103–112.
76. Zemanick MC, Strick PL, Dix RD. Direction of transneuronal transport of herpes simplex virus 1 in the primate motor system is strain-dependent. Proc Natl Acad Sci USA 1991; 88: 8048–8051.
77. Rinaman L, Schwartz GJ. Anterograde transneuronal viral tracing of central viscerosensory pathways in rats. J Neurosci 2004; 24: 2782–2786.
78. Song CK, Schwartz GJ, Bartness TJ. Anterograde transneuronal viral tract tracing reveals central sensory circuits from white adipose tissue. Am J Physiol Regul Integr Comp Physiol 2009; 296: R501–R511.
79. Song CK, Bartness TJ. Central Projections of the Sensory Nerves Innervating Brown Adipose Tissue. Society for Neuroscience: Neuroscience Meeting Planner San Diego, CA, Online 2007.
80. Song CK, Smith B, Nguyen N, Bartness TJ. Convergence of Efferent and Afferent Circuits to White Adipose Tissue in Siberian Hamsters. Society for Neuroscience: Neuroscience Meeting Planner Chicago, IL, Online 2009.
81. Borzan J, LaGraize SC, Hawkins DL, Peng YB. Dorsal horn neuron response patterns to graded heat stimuli in the rat. Brain Res 2005; 1045: 72–79.
82. Iggo A. Cutaneous thermoreceptors in primates and subprimates. J Physiol 1969; 200: 403–430.
83. Cinti S. The Adipose Organ. Editrice Kurtis: Milano, 1999.
84. Matthias A, Ohlson KB, Fredriksson JM, Jacobsson A, Nedergaard J, Cannon B. Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty acid-induced thermogenesis. J Biol Chem 2000; 275: 25073–25081.
85. Brasaemle DL. Thematic review series: Adipocyte biology. The perilipin family of structural lipid droplet proteins: Stabilization of lipid droplets and control of lipolysis. J Lipid Res 2007; 48: 2547–2559.
86. Souza SC, Christoffolete MA, Ribeiro MO, Miyoshi H, Strissel KJ, Stancheva ZS, Perilipin regulates the thermogenic actions of norepinephrine in brown adipose tissue. J Lipid Res 2007; 48: 1273–1279.