Anterograde transneuronal viral tract tracing reveals central sensory circuits from white adipose tissue

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 3, 2009, Pages

  Song, C Kay ^a   Schwartz, Gary J ^b   Bartness, Timothy J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

2 deoxy D glucose; Electrophysiology; Lipolysis; Sympathetic nervous system

Indexed keywords

DEOXYGLUCOSE; ANTIMETABOLITE;

ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EPIDIDYMIS; FEEDBACK SYSTEM; HERPES SIMPLEX VIRUS 1; IMMUNOREACTIVITY; LIPID METABOLISM; LIPOLYSIS; MALE; NERVE CELL; NERVE FIBER; NONHUMAN; PHODOPUS; PRIORITY JOURNAL; SENSORY NERVE CELL; SPIKE WAVE; SPINAL GANGLION; WHITE ADIPOSE TISSUE; ACTION POTENTIAL; ANIMAL; BRAIN; CYTOLOGY; HAMSTER; HERPES SIMPLEX; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INNERVATION; NODOSE GANGLION; PATHOLOGY; PERIPHERAL NERVE; PHYSIOLOGY; SENSORY NERVE; STATISTICAL ANALYSIS;

ACTION POTENTIALS; ADIPOSE TISSUE, WHITE; AFFERENT PATHWAYS; ANIMALS; ANTIMETABOLITES; BRAIN; CRICETINAE; DATA INTERPRETATION, STATISTICAL; DEOXYGLUCOSE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBERS; NEURONS, AFFERENT; NODOSE GANGLION; PERIPHERAL NERVES; PHODOPUS;

EID: 64149123008     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90786.2008     Document Type: Article

References (50)

1. Arch JR. Central regulation of energy balance: inputs, outputs and leptin resistance. Proc Nutr Soc 64: 39-46, 2005.
2. Ballantyne B. Histochemical and biochemical aspects of cholinesterase activity of adipose tissue. Arch Int Pharmacodyn Ther 173: 343-350, 1968.
3. 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. (Pubitemid 28376320)
4. Bamshad M, Song CK, Bartness TJ. CNS origins of the sympathetic nervous system outflow to brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 276: R1569-R1578, 1999. (Pubitemid 29323518)
5. Banks WA, Kastin AJ, Huang WT, Jaspan JB, Maness LM. Leptin enters the brain by a saturable system independent of insulin. Peptides 17: 305-311, 1996.
6. Barnett EM, Evans GD, Sun N, Perlman S, Cassell MD. Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1. J Neurosci 15: 2972-2984, 1995.
7. 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.
8. Bartness TJ, Song CK. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res 48: 1655-1672, 2007.
9. Baskin DG, Lattemann DF, Seeley RJ, Woods SC, Porte D Jr, Schwartz MW. Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res 848: 114-123, 1999.
10. Brito MN, Brito NA, Baro DJ, Song CK, Bartness TJ. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148: 5339-53347, 2007.
11. Brito NA, Brito MN, Bartness TJ. Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am J Physiol Regul Integr Comp Physiol 294: R1445-R1452, 2008.
12. Cervero F, Foreman RD. Sensory innervation of the viscera. In: Central Regulation of Autonomic Functions, edited by Loewy AD and Spyer KM. New York: Oxford University Press, 1990, p. 104-125.
13. Cinti S. The Adipose Organ. Milano, Italy: Editrice Kurtis, 1999.
14. Cottrell DF, Iggo A. Tension receptors with vagal afferent fibres in the proximal duodenum and pyloric sphincter of sheep. J Physiol 354: 457-475, 1984. (Pubitemid 14066379)
15. Cowley AW Jr. Long-term control of arterial blood pressure. Physiol Rev 72: 231-300, 1992.
16. Dark J, Miller DR, Zucker I. Reduced glucose availability induced torpor in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 267: R496-R501, 1994. (Pubitemid 2132696)
17. 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 40: 103-112, 1983.
18. Fishman RB, Dark J. Sensory innervation of white adipose tissue. Am J Physiol Regul Integr Comp Physiol 253: R942-R944, 1987. (Pubitemid 18027271)
19. Fox EA, Powley TL. Longitudinal columnar organization within the dorsal motor nucleus represents separate branches of the abdominal vagus. Brain Res 341: 269-282, 1985.
20. 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.
21. Havel PJ. Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp Biol Med (Maywood ) 226: 963-977, 2001.
22. Helke CJ, Charlton CG, Wiley RG. Studies on the cellular localization of spinal cord substance P receptors. Neuroscience 19: 523-533, 1986.
23. Kalia M, Sullivan JM. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211: 248-265, 1982. (Pubitemid 13247365)
24. Kennedy GC. The role of depot fat in the hypothalamic control of food intake in the rat. Proc R Soc Lond B 140: 578-592, 1953.
25. 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. Selective parasympathetic innervation of subcutaneous and intra-abdominal fat-functional implications. J Clin Invest 110: 1243-1250, 2002. (Pubitemid 35285750)
26. Kreier F, Kap YS, Mettenleiter TC, van HC, van d V, Kalsbeek A, Sauerwein HP, Fliers E, Romijn JA, Buijs RM. Tracing from fat tissue, liver, and pancreas: a neuroanatomical framework for the role of the brain in type 2 diabetes. Endocrinology 147: 1140-1147, 2006.
27. Lal S, Kirkup AJ, Brunsden AM, Thompson DG, Grundy D. Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol 281: G907-G915, 2001. (Pubitemid 32953148)
28. Langin D, Portillo MP, Saulnier-Blache JS, Lafontan M. Coexistence of three beta-adrenoceptor subtypes in white fat cells of various mammalian species. Eur J Pharm 199: 291-301, 1991.
29. Melone J. Vagal receptors sensitive to lipids in the small intestine of the cat. J Auton Nerv Syst 17: 231-241, 1986. (Pubitemid 17170447)
30. Naito C, Yoshitoshi Y, Higo K, Ookawa H. Effects of long-term administration of 2-deoxy-D-glucose on food intake and weight gain in rats. J Nutr 103: 730-737, 1973.
31. Newsholme EA, Leech AR. Biochemistry for the Medical Sciences. Chichester, UK: John Wiley, 1983.
32. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2001.
33. Rinaman L, Schwartz GJ. Anterograde transneuronal viral tracing of central viscerosensory pathways in rats. J Neurosci 24: 2782-2786, 2004. (Pubitemid 38380955)
34. Schwartz GJ, McHugh PR, Moran TH. Pharmacological dissociation of responses to CCK and gastric loads in rat mechanosensitive vagal afferents. Am J Physiol Regul Integr Comp Physiol 267: R303-R308, 1994.
35. Shaw JE, Ramwell PW. Release of prostaglandin from rat epididymal fat pad on nervous and hormonal stimulation. J Biol Chem 243: 1498-1503, 1968.
36. Shi H, Bartness TJ. Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Res Bull 54: 375-385, 2001. (Pubitemid 32288718)
37. 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 Regul Integr Comp Physiol 288: R1028-R1037, 2005. (Pubitemid 40404180)
38. Smith JA, Amagasu SM, Eglen RM, Hunter JC, Bley KR. Characterization of prostanoid receptor-evoked responses in rat sensory neurones. Br J Pharmacol 124: 513-523, 1998.
39. 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.
40. Song CK, Enquist LW, Bartness TJ. New developments in viral tracings of neural circuits. Virus Res 11: 235-249, 2005.
41. 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. (Pubitemid 41507413)
42. 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 Regul Integr Comp Physiol 295: R417-R428, 2008.
43. Sun N, Cassell MD, Perlman S. Anterograde, transneuronal transport of herpes simplex virus type 1 strain H129 in the murine visual system. J Virol 70: 5405-5413, 1996. (Pubitemid 26240714)
44. Wang Y, Lobstein T. Worldwide trends in childhood overweight and obesity. Int J Pediatr Obes 1: 11-25, 2006.
45. Willis WD, Coggeshall RE. Sensory Mechanisms of the Spinal Cord. New York: Plenum Press, 1991.
46. Wirtshafter D, Davis JD. Set points, settling points, and the control of body weight. Physiol Behav 19: 75-78, 1977. (Pubitemid 8228465)
47. Yamamoto K, Senba E, Matsunaga T, Tohyama M. Calcitonin gene-related peptide containing sympathetic preganglionic and sensory neurons projecting to the superior cervical ganglion of the rat. Brain Res 487: 158-164, 1989. (Pubitemid 19135178)
48. Youngstrom TG, Bartness TJ. Catecholaminergic innervation of white adipose tissue in the Siberian hamster. Am J Physiol Regul Integr Comp Physiol 268: R744-R751, 1995.
49. Youngstrom TG, Bartness TJ. White adipose tissue sympathetic nervous system denervation increases fat pad mass and fat cell number. Am J Physiol Regul Integr Comp Physiol 275: R1488-R1493, 1998.
50. 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 88: 8048-8051, 1991.