Sensory or sympathetic white adipose tissue denervation differentially affects depot growth and cellularity

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 4 57-4, 2005, Pages

  Shi, Haifei ^a   Song, C Kay ^a   Giordano, Antonio ^b   Cinti, Saverio ^b   Bartness, Timothy J ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Calcitonin gene related peptide; Capsaicin; Immunohistochemistry; Surgical denervation; Tyrosine hydroxylase

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL SIZE; DENERVATION; EPIDIDYMIS FAT; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INGUINAL REGION; MALE; MICROINJECTION; NONHUMAN; PHODOPUS; PRIORITY JOURNAL; SENSORY NERVE; SYMPATHETIC INNERVATION; WHITE ADIPOSE TISSUE;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CAPSAICIN; CELL SIZE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRICETINAE; DENERVATION; IMMUNOHISTOCHEMISTRY; MALE; NEURONS, AFFERENT; NOREPINEPHRINE; PHODOPUS; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; SYMPATHETIC NERVOUS SYSTEM; TYROSINE 3-MONOOXYGENASE;

EID: 15544385323     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00648.2004     Document Type: Article

References (53)

1. Ainsworth A, Halim P, Wall PD, Allt G, Mackenzie M, Gibson S, and Polak J. 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, 1981.
2. Atgie C, Le Gouic S, Marti L, Hanoun N, Casteilla L, Penicaud L, Ambid L, and Carpene C. Lipolytic and antilipolytic responses of the Siberian hamster (Phodopus sungorus sungorus) white adipoctyes after weight loss induced by short photoperiod exposure. Comp Biochem Physiol 119A: 503-510, 1998.
3. Bamshad M, Aoki VT, Adkison MG, Warren WS, and 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.
4. Bartness TJ. Dual innervation of white adipose tissue: some evidence for parasympathetic nervous system involvement. J Clin Invest 110: 1235-1237, 2002.
5. Bartness TJ. Animal and body fat changes: measurement and interpretation. In: Methods and Techniques to Study Feeding and Drinking Behavior, edited by Toates FM and Rowland NE. Amsterdam: Elsevier, 1987, p. 463-498.
6. Bartness TJ and 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.
7. Bartness TJ, Demas GE, and Song CK. Central nervous system innervation of white adipose tissue. In: Adipose Tissue, edited by Klaus S. Georgetown, TX: Landes Bioscience, 2001, p. 116-130.
8. Beznak ABL and Hasch Z. The effect of sympathectomy on the fatty deposit in connective tissue. Q J Exp Physiol 27: 1-15, 1937.
9. Bouloumie A, Planat V, Devedjian JC, Valet P, Saulnier-Blache JS, Record M, and Lafontan M. α2-Adrenergic stimulation promotes preadipocyte proliferation. Involvement of mitogen-activated protein kinases. J Biol Chem 269: 30254-30259, 1994.
10. Bowers RR, Festuccia WTL, Song CK, Shi H, Migliorini RH, and Bartness TJ. Sympathetic innervation of white adipose tissue and its regulation of fat cell number. Am J Physiol Regul Integr Comp Physiol 286: R1167-R1175, 2004.
11. Bray GA and Nishizawa Y. Ventromedial hypothalamus modulates fat mobilisation during fasting. Nature 274: 900-901, 1978.
12. Cantu RC and Goodman HM. Effects of denervation and fasting on white adipose tissue. Am J Physiol 212: 207-212, 1967.
13. Cinti S. The Adipose Organ. Milano: Editrice Kurtis, 1999.
14. Clement G. 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. Arch Sci Physiol (Paris) 4: 13-29, 1950.
15. Cousin B, Casteilla L, Lafontan M, Ambid L, Langin D, Berthault MF, and Penicaud L. Local sympathetic denervation of white adipose tissue in rats induces preadipocyte proliferation without noticeable changes in metabolism. Endocrinology 133: 2255-2262, 1993.
16. Cui J and Himms-Hagen J. Long-term decrease in body fat and in brown adipose tissue in capsaicin-desensitized rats. Am J Physiol Regul Integr Comp Physiol 262: R568-R573, 1992.
17. Demas GE and Bartness TJ. Novel method for localized, functional sympathetic nervous system denervation of peripheral tissue using guanethidine. J Neurosci Methods 112: 21-28, 2001.
18. Demas GE and Bartness TJ. Direct innervation of white fat and adrenal medullary catecholamines mediate photoperiodic changes in body fat. Am J Physiol Regul Integr Comp Physiol 281: R1499-R1505, 2001.
19. Dieudonne MN, Pecquery R, Leneveu MC, Jaubert AM, and Giudicelli Y. Androgen receptors in cultured rat adipose precursor cells during proliferation and differentiation: regional specificities and regulation by testosterone. Endocrinology 3: 537-541, 1995.
20. DiGirolamo M, Fine JB, Tagra K, and Rossmanith R. Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol Regul Integr Comp Physiol 274: R1460-R1467, 1998.
21. Dogiel AS. Die sensiblen Nervenendigungen im Herzen und in den Blutgefassen der Saugethiere. Arch mikr Anat 52: 44-70, 1898.
22. Faust IM. Role of the fat cell in energy balance physiology. In: Eating and Its Disorders, edited by Stunkard AJ and Stellar E. New York: Raven, 1984, p. 97-107.
23. Fishman RB and Dark J. Sensory innervation of white adipose tissue. Am J Physiol Regul Integr Comp Physiol 253: R942-R944, 1987.
24. Giordano A, Morroni M, Carle F, Gesuita R, Marchesi GF, and Cinti S. Sensory nerves affect the recruitment and differentiation of rat periovarian brown adipocytes during cold acclimation. J Cell Sci 111: 2587-2594, 1998.
25. Giordano A, Morroni M, Santone G, Marchesi GF, and 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 25: 125-136, 1996.
26. Hirsch J and Gallian E. Methods for the determination of adipose cell size in man and animals. J Lipid Res 9: 110-119, 1968.
27. Jones DD, Ramsay TG, Hausman GJ, and Martin RJ. Norepinephrine inhibits rat pre-adipocyte proliferation. Int J Obes 16: 349-354, 1992.
28. Kirtland J and Gurr MI. Adipose tissue cellularity: a review. 2. The relationship between cellularity and obesity. Int J Obes 3: 15-55, 1979.
29. Kreier F, Fliers E, Voshol PJ, Van Eden CG, Havekes LM, Kalsbeek A, Van Heijningen CL, Sluiter AA, Mettenleiter TC, Romijn JA, Sauerwein HP, and Buijs RM. Selective parasympathetic innervation of subcutaneous and intra-abdominal fat-functional implications. J Clin Invest 110: 1243-1250, 2002.
30. Lafontan M and Berlan M. Fat cell adrenergic receptors and the control of white and brown fat cell function. J Lipid Res 34: 1057-1091, 1993.
31. 2-adrenoceptors: the regulation of fat cell function and lipolysis. Endocr Rev 16: 716-738, 1995.
32. 2-antagonists and lipid-mobilizing strategies. Am J Clin Nutr 55: 219S-227S, 1992.
33. Mauer MM and Bartness TJ. Temporal changes in fat pad mass following lipectomy in Siberian hamsters. Physiol Behav 62: 1029-1036, 1997.
34. Mauer MM, Harris RBS, and Bartness TJ. The regulation of total body fat: lessons learned from lipectomy studies. Neurosci Biobehav Rev 25: 15-28, 2001.
35. Mefford IN. Application of high performance liquid chromatography with electrochemical detection to neurochemical analysis: measurement of catecholamines, serotonin and metabolites in rat brain. J Neurosci Methods 3: 207-224, 1981.
36. Melnyk A and Himms-Hagen J. Leanness in capsaicin-desensitized rats one year after treatment (Abstract). Int J Obes 18, Suppl 1: 130, 1994.
37. Newsholme EA and Leech AR. Biochemistry for the Medical Sciences. Chichester, UK: Wiley, 1983.
38. Niijima A. Reflex effects from leptin sensors in the white adipose tissue of the epididymis to the efferent activity of the sympathetic and vagus nerve in the rat. Neurosci Lett 262: 125-128, 1999.
39. Nishizawa Y and Bray GA. Ventromedial hypothalamic lesions and the mobilization of fatty acids. J Clin Invest 61: 714-721, 1978.
40. Raybould HE, Sternini C, Eysselein VE, Yoneda M, and Holzer P. Selective ablation of spinal afferent neurons containing CGRP attenuates gastric hyperemic response to acid. Peptides 13: 249-254, 1992.
41. Raybould HE and Tache Y. Cholecystokinin inhibits gastric motility and emptying via a capsaicin-sensitive vagal pathway in rats. Am J Physiol Gastrointest Liver Physiol 255: G242-G246, 1988.
42. Schwob JE, Szumowski KEM, and Stasky AA. Olfactory sensory neurons are trophically dependent on the olfactory bulb for their prolonged survival. J Neurosci 12: 3896-3919, 1992.
43. Shi H and Bartness TJ. Neurochemical phenotype of sympathetic nervous system outflow from brain to white fat. Brain Res Bull 54: 375-385, 2001.
44. Shi H, Bowers RR, and Bartness TJ. Norepinephrine turnover in brown and white adipose tissue after partial lipectomy. Physiol Behav 81: 535-543, 2004.
45. Skofitsch G and Jacobowitz DM. Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 6: 747-754, 1985.
46. Takahashi A, Ikarashi Y, Ishimaru H, and Maruyama Y. Compensation between sympathetic nerves and adrenal medullary activity: effects of adrenomedullation and chemical sympathectomy on catecholamine turnover. Life Sci 53: 1567-1572, 1993.
47. Teixeira VL, Antunes-Rodrigues J, and Migliorini RH. Evidence for centers in the central nervous system that selectively regulate fat mobilization in the rat. J Lipid Res 14: 672-677, 1973.
48. Valet P, Pages C, Jeanneton O, Daviaud D, Barbe P, Record M, Saulnier-Blache JS, and Lafontan M. α2-Adrenergic receptor-mediated release of lysophosphatidic acid by adipocytes. A paracrine signal for preadipocyte growth. J Clin Invest 101: 1431-1438, 1998.
49. Wade GN. Actions of gonadal steroids on adipose tissues in rodents. In: Metabolic Complications of Human Obesities, edited by Vague J. New York: Elsevier, 1985, p. 105-114.
50. White JE and Engel FL. A lipolytic action of epinephrine and norepinephrine on rat adipose tissue in vitro. Proc Soc Exp Biol Med 99: 375-378, 1958.
51. Wright JT and Hausman GJ. Monoclonal antibodies against cell surface antigens expressed during porcine adipocyte differentiation. Int J Obes 14: 284-291, 1990.
52. Youngstrom TG and Bartness TJ. Catecholaminergic innervation of white adipose tissue in the Siberian hamster. Am J Physiol Regul Integr Comp Physiol 268: R744-R751, 1995.
53. Youngstrom TG and 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.