Sensory nerves affect the recruitment and differentiation of rat periovarian brown adipocytes during cold acclimation

Journal of Cell Science

Volumn 111, Issue 17, 1998, Pages 2587-2594

  Giordano, Antonio ^a   Morroni, Manrico ^a   Carle, Flavia ^a   Gesuita, Rosaria ^a   Marchesi, Gian Franco ^a   Cinti, Saverio ^a,b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b Facoltà di Medicina   (Italy)

Author keywords

Brown adipocyte; Capsaicin desensitization; Periovarian adipose tissue; Precursor; Rat; Recruitment; Sensory nerve

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; NEUROPEPTIDE Y; SUBSTANCE P;

ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; COLD ACCLIMATIZATION; DESENSITIZATION; FEMALE; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; RAT; SENSORY NERVE;

ACCLIMATIZATION; ADIPOCYTES; ADIPOSE TISSUE, BROWN; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; CELL COUNT; CELL DIFFERENTIATION; COLD; FEMALE; MICROSCOPY, ELECTRON; NEURONS, AFFERENT; NEUROPEPTIDES; OVARY; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANCE P; TEMPERATURE;

EID: 0031711172     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Bjorntorp, P. (1996). The regulation of adipose tissue distribution in humans. Int. J. Obesity 20, 291-302.
2. Boss, O., Samec, S., Paoloni-Giacobino, A., Rosser, C., Dulloo, A., Seydoux, J., Muzzin, P. and Giacobino, J.-P. (1997). Uncoupling protein3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Lett. 408, 39-42.
3. Bradley, J. V. (1968). Distribution Free Statistical Tests. Prentice-Hall, London.
4. Brain, S. D., Williams, T. J., Tippins, J. R., Morris, H. R. and MacIntyre, I. (1985). Calcitonin gene-related peptide is a potent vasodilator. Nature 313, 54-56.
5. Cannon, B., Bengtsson, T., Dicker, A., Jacobsson, A., Kuusela, P., Thonberg, H., Tvrdik, P., Zhao, J. and Nedergaard, J. (1994). The role of adrenergic stimulation in regulation of heat production and recruitment of brown adipose tissue. In Thermal Balance in Health and Disease (ed. E. Zeisberger, E. Schonbaum and P. Lomax), pp. 87-102. Birkhauser Verlag, Basel.
6. Casini, A., Galli, G., Salzano, R., Santicioli, P., Maggi, C. A., Rotella, C. M. and Surrenti, C. (1991). Calcitonin gene-related peptide increased the production of glycosaminoglycans but not of collagen type I and III in cultures of rat fat-storing cells. Life Sci. 49, PL163-PL168.
7. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D. and Julius, D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824.
8. Cervero, F. and McRitchie, H. A. (1982). Neonatal capsaicin does not affect umnyelimited efferent fibers of the autonomie nervous system: functional evidence. Brain Res. 239, 283-288.
9. Champion, H. C. and Kadowitz, P. J. (1997). Vasodilator responses to acetylcholine, bradykinin. and substance P are mediated by TEA-sensitive mechanism. Am. J. PHysiol. 273, R414-R422.
10. Cinti, S. (1992). Morphological and functional aspects of brown adipose tissue. In The Obese Child, vol. 2 (ed. P. L. Giorgi, R. M, Suskind and C. Catassi), pp. 125-132, Karger, Basel.
11. Cinti, S., Zancanaro, C., Sbarbati, A., Cigolini, M., Vogel, P., Ricquier, D. and Kakan, S. (1989). Immunoelectron microscopical identification of the uncoupling protein in brown adipose tissue mitochondria. Biol. Cell 67, 359-362.
12. Cormarèche-Leydier, M., Shimada, S. G., Stitt, J. T. (1985). Hypothalamic thermosensitivity in capsaicin-desensitized rats. J. Physiol. Lond. 363, 227236.
13. Cousin, B., Cinti, S., Morroni, M., Raimbault, S., Ricquier, D., Penioaud, L. and Casteilla, L. (1992). Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J. Cell Sci. 103, 931-942.
14. Cousin, B., Casteilla, L., Dani, C., Muzzin, P., Revelli, J. P. and Penicaud, L. (1993). Adipose tissues from various anatomical sites are characterized by different patterns of gene expression and regulation. Bioclicm. J. 292, 873-876.
15. Cousin, B., Bascands-Viguurie, N., Kassis, N., Nibbelink, M., Ainbid, L., Casteilla, L. and Penicaud, L. (1996). Cellular changes during cold acclimatation in adipose tissues. J. Cell Physiol. 167, 285-289.
16. Cui, J., Zaror-Behrens, G. and Himms-Hagcn, J. (1990). Capsaicin descnsitization induces atrophy of brown adipose tissue in rats. Am. J. Physiol. 259, R324-R332.
17. Cui, J. and Himms-Hagen, J. (1992a). Rapid but transient atrophy of brown adipose tissue in eapsaiein-desensitized rats. Am. J. Phvsiol. 262. R562-R567.
18. Cui, J. and Himms-Hagen, J. (1992b). Long-term decrease in body fat and in brown adipose tissue in eapsaicin-desensitized rats. Am. J. Physiol, 262. R568-R573.
19. Denis-Donini, S. (1989). Expression of dopaminergic phenotypes in the mouse olfactory bulb induced by the calcitonin gene-related peptide. Nature 339, 701-703.
20. Fishman, R. B. and Dark, J. (1987). Sensory innervation of white adipose tissue. Am. J. Physiol. 253, R942-R944.
21. Fitzgerald, M. (1983). Capsaicin and sensory neurones - a review. Pain 15, 108-130.
22. Fleury, C., Neverova, M., Collins, S., Raimbault, S., Champigny, O., Levi-Meyrueis, C., Bouillaud, F., Seldin, M. F., Surwit, R. S., Ricquier, D. and Warden, C. H. (1997). Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nature Genetics 15, 269-272.
23. Gibson, S. J., Polak, J. M., Bloom, S. R., Sabate, I. M., Mulderry, P. M., Ghatei, M. A., McGregor, G. P., Morrison, J. E. B., Kelly, J. S., Evans, R. M. and Rosenfeld, M. G. (1984). Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and eight other species. J. Neumsci. 4, 3101-3111.
24. Giordann, A., Morroni, M., Santone, G., Marchesi, G. F. and Cinti, S. (1996). Tyrosine hydroxylase, neuropeptidc Y. substance P, calcitonin generelated peptide and vasoactive intestinal peptide in nerves of rat periovarian adipose tissue: an immunohistochemieai and ultrastructural investigation. J. Neurocytol. 25, 125-136.
25. Girardier, L. and Stock, M. J. (1983). Mammalian Thennogenesis. Chapman and Hall, London.
26. Haegerstrand, A., Dalsgaard, C.-J., Jonzon, B., Larsson, O. and Nilsson, J. (1990). Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc. Nat. Acad. Sci. USA 87, 3299-3303.
27. Himms-Hagen, J., Cui, J. and Sigurdson, S. L. (1990). Sympathetic and sensory nerves in control of growth of brown tissue: effects of denervation and of capsaicin. Neurochem. Intern. 17, 271-279.
28. Holzer, P. (1988). Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24, 739-768.
29. Holzer, P. (1991). Capsaicin: cellular targets, mechanism of action, and selectivity forthin sensory neurons. Pharmacol. Rev. 43, 143-201.
30. Hori, T. (1984). Capsaicin and central control of thermoregulation. Pharmacol. Ther. 26, 389-416.
31. Hsu, S. M., Raine, L. and Fanger, H. (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP procedures). J. Histochem. Cytochem. 29, 577-580.
32. Jancso, G., Kiraly, E. and Jancso-Cabor, A. (1977). Pharmacologically induced selective degeneration of ehemoscnsitive primary neurons. Mature 270, 741-743.
33. Lee, V., Kaway, Y., Shiosaka, S., Takami, K., Kiyama, H., Hylliard, C. J., McIntyre, I., Emson, P. C. and Tonyama, M. (1986). Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: Immunohisiochemicul analysis. Brain Res, 330, 194-196.
34. Leighton, B. and Foot, E. A. (1995). The role of the sensory pepide calcitonin gene-related peptide(s) in skeletal muscle carbohydrate metabolism: effects of capsaicin and resiniteratoxin. Biochem. J. 307, 707-712.
35. Lowell, B., Susulic, V., Hamann, A., Lawitts, J., Himms-Hapen, J., Boyers, B., Kozak, L. and Flier, J. (1993). Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature 336, 740-742.
36. Maggi, C. A. (1995). Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 45, 1-98.
37. Maggi, C. A. and Meli, A. (1988). The sensory-efferent function of capsaicinsensitive sensory neuron. Gen. Pharmac. 19, 1-43.
38. Mitsuhashi, M. and Payan, D. G. (1987). The mitogenic effects of vasoactive neuropeptides on cultured smooth muscle cell lines. Life Sci. 40, 853-861.
39. Narumi, S. and Maki, Y. (1978). Stimulatory effects of substance P on neurite extension and cyclic AMP levels in cultured neuroblastoma cells. J. Neurochem. 30, 1321-1326.
40. Nilsson, J., von Euler, A. M. and Dalsgaard, C.-J. (1985). Stimulation of connective tissue cell growth by substance P and substance K. Nature 315, 61-63.
41. Nisoli, E., Tonello, C., Briscini, L. and Carruba, M. (1997). Indueible nitric oxide synthase in rat brown adipocytes; Implications for blood flow to brown adipose tissue. Endocrinology 138, 676-682.
42. Norman, D., Mukherjee, S., Symons, D., Jung, R. T. and Lever, J. D. (1988). Neuropeptides in interscapular and perirenal brown adipose tissue in the rat: a plurality of innervation. J. Neurocytol. 17, 305-311.
43. Ribiere, C., Jaubert, A. M., Gaudiot, N., Sabourault, D., Marcus, M. L., Boucher, J. L., Denis-Henriot, D. and Giudicelli, Y. (1996). White adipose tissue nitric oxide synthase: a potential source for NO production. Bittehem. Biophys. Res. Commun. 222, 706-712.
44. Skofitsch, F. and Jacobowitz, D. M. (1985). Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 6, 747-754.
45. Takano, Y., Nagashima, A., Kamiya, H., Kurosawa, M. and Sato, A. (1988). Well-maintained reflex responses of sympathetic nerve activity to stimulation of baroreceptor, chemoreceptor and cutaneous mechanoreceptors in neonatal capsaicin-treated rats. Brain Res. 444, 188-192.
46. Terenghi, G., Polak, J. M., Ghatei, M. A., Mulderry, P. K., Butler, J. M., Unger, W. G. and Bloom, S. R. (1985). Distribution and origin of CGRP-immunoreactivity in the sensory innervation of the mammalian eye. J, Comp. Neurol. 233, 505-516.
47. Trayhurn, P. and Nicholls, D. G. (1986). Brown Adipose Tissue. Edward Arnold, London.
48. Young, P., Arch, J. R. S. and Ashwell, M. (1984). Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett. 167, 10-14.