Hostname: page-component-6b989bf9dc-vmcqm Total loading time: 0 Render date: 2024-04-12T10:42:26.376Z Has data issue: false hasContentIssue false

The adipose organ: morphological perspectives of adipose tissues

Published online by Cambridge University Press:  05 March 2007

Saverio Cinti*
Affiliation:
Institute of Normal Human Morphology-Anatomy, Faculty of Medicine, University of Ancona, Via Tronto 10/A, 60020 Ancona, Italy
*
Corresponding author: Professor Saverio Cinti, fax +39 071 2206087, email cinti@popcsi.unian.it
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.

Anatomically, an organ is defined as a series of tissues which jointly perform one or more interconnected functions. The adipose organ qualifies for this definition as it is made up of two tissue types, the white and brown adipose tissues, which collaborate in partitioning the energy contained in lipids between thermogenesis and the other metabolic functions. In rats and mice the adipose organ consists of several subcutaneous and visceral depots. Some areas of these depots are brown and correspond to brown adipose tissue, while many are white and correspond to white adipose tissue. The number of brown adipocytes found in white areas varies with age, strain of animal and environmental conditions. Brown and white adipocyte precursors are morphologically dissimilar. Together with a rich vascular supply, brown areas receive abundant noradrenergic parenchymal innervation. The gross anatomy and histology of the organ vary considerably in different physiological (cold acclimation, warm acclimation, fasting) and pathological conditions such as obesity; many important genes, such as leptin and uncoupling protein-1, are also expressed very differently in the two cell types. These basic mechanisms should be taken into account when addressing the physiopathology of obesity and its treatment.

Type
Symposium on ‘New perspectives on adipose tissue function’
Copyright
Copyright © The Nutrition Society 2001

References

Ailhaud, G, Dani, C, Gaillard, D, Grimaldi, P & Negrel, R (1992) Critical steps and hormonal control of adipose cell differentiation. In The Obese Child, vol. 2, pp. 115124 [Giorgi, PL, Suskind, RM and Catassi, C, editors]. Basel: Karger.Google Scholar
Arch, JRS & Kaumann, AJ (1993) Beta3 and atypical beta-adrenoceptors. Medical Research Review 13, 663729.Google Scholar
Barbatelli, G, Heinzelmann, M, Ferrara, P, Morroni, M & Cinti, S (1994) Quantitative evaluations of gap junctions in old rat brown adipose tissue after cold acclimation: a freezefracture and ultrastructural study. Tissue and Cell 26, 667676.CrossRefGoogle Scholar
Barbatelli, G, Morroni, M, Vinesi, P, Cinti, S & Michetti, F (1993) S-100 protein in rat brown adipose tissue under different functional conditions: A morphological, immunocytochemical, and immunochemical study. Experimental Cell Research 208, 226231.CrossRefGoogle ScholarPubMed
Blanchette-Mackie, EJ & Scow, RO (1981) Lipolysis and lamellar structures in white adipose tissue of young rats: lipid movement in membranes. Journal of Ultrastructural Research 77, 295318.CrossRefGoogle ScholarPubMed
Blanchette-Mackie, EJ & Scow, RO (1983) Movement of lipolytic products to mitochondria in brown adipose tissue of young rats: an electron microscope study. Journal of Lipid Research 24, 229244.CrossRefGoogle ScholarPubMed
Boss, O, Samec, S, Paoloni-Giacobino, A, Rossier, C, Dulloo, A, Seydoux, J, Muzzin, P & Giacobino, J-P (1997) Uncoupling protein 3: a new member of the mitochondrial carrier family with tissue-specific expression. FEBS Letters 408, 3942.CrossRefGoogle ScholarPubMed
Cancello, R, Zingaretti, MC, Sarzani, R, Ricquier, D & Cinti, S (1998) Leptin and UCP1 genes are reciprocally regulated in brown adipose tissue. Endocrinology 139, 47474750.CrossRefGoogle ScholarPubMed
Cannon, B, Hedin, A & Nedergaard, J (1982) Exclusive occurrence of thermogenin antigen in brown adipose tissue. FEBS Letters 150, 129132.Google Scholar
Cannon, B, Nedergaard, J, Lundberg, JM, Hokfelt, T, Terenius, L & Goldstein, M (1986) ‘Neuropeptide tyrosine’ (NPY) is co-stored with noradrenaline in vascular but not in parenchymal sympathetic nerves of brown adipose tissue. Experimental Cell Research 164, 546550.CrossRefGoogle Scholar
Casanueva, FF & Dieguez, C (1999) Neuroendocrine regulation and actions of leptin. Frontiers in Neuroendocrinology 20, 317363.Google Scholar
Caterina, MJ, Schumaker, MA, Tominaga, M, Rosen, TA, Levine, JD & Julius, D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816824.Google Scholar
Cigolini, M, Cinti, S, Bosello, O, Brunetti, L & Bjorntorp, P (1986) Isolation and ultrastructural features of brown adipocytes in culture. Journal of Anatomy 145, 207216.Google Scholar
Cigolini, M, Cinti, S, Brunetti, L, Bosello, O, Osculati, F & Bjorntorp, P (1985) Human brown adipose cells in culture. Experimental Cell Research 159, 261266.CrossRefGoogle ScholarPubMed
Cinti, S (1999) The Adipose Organ. Milan, Italy: Editrice Kurtis.Google Scholar
Cinti, S, Cigolini, M, Bosello, O & Bjorntorp, P (1984) A morphological study of the adipocyte precursor. Journal of Submicroscopic Cytology 16, 243251.Google ScholarPubMed
Cinti, S, Cigolini, M, Gazzanelli, G & Bosello, O (1985) An ultrastructural study of adipocyte precursors from epididymal fat pads of adult rats in culture. Journal of Submicroscopic Cytology 17, 631636.Google Scholar
Cinti, S, Cigolini, M, Morroni, M & Zingaretti, MC (1989a) S-100 protein in white preadipocytes: an immunoelectronmicroscopic study. Anatomical Record 224, 466472.CrossRefGoogle ScholarPubMed
Cinti, S, Cigolini, M, Sbarbati, A & Zancanaro, C (1986) Ultrastructure of brown adipocytes mitochondria in cell culture from explants. Journal of Submicroscopic Cytology 18, 625627.Google ScholarPubMed
Cinti, S, Cigolini, M, Sbarbati, A, Zancanaro, C & Bjorntorp, P (1987) Effects of noradrenaline exposure on rat brown adipocytes in cultures. An ultrastructural study. Tissue and Cell 19, 809816.CrossRefGoogle ScholarPubMed
Cinti, S, De Matteis, R, Zingaretti, MC, Cancello, R, Himms-Hagen, J & Ricquier, D (1997a) Harlequin's secret: UCP-immunostained brown adipose tissue. International Journal of Obesity 21, Suppl. 2, S47.Google Scholar
Cinti, S, De Matteis, R, Zingaretti, MC & Himms-Hagen, J (1997b) Immunohistochemical localization of leptin in adipose tissues. In Leptin – The Voice of Adipose Tissue, pp. 7882 [Blum, WK, Kiess, W, Rascher, W and Barth, JA, editors]. Heidelberg, Germany: JA Barth Verlag.Google Scholar
Cinti, S, Frederich, RC, Zingaretti, MC, De Matteis, R, Flier, JS & Lowell, BB (1997 c) Immunohistochemical localization of leptin and uncoupling protein in white and brown adipose tissue. Endocrinology 138, 797804.CrossRefGoogle ScholarPubMed
Cinti, S, Zancanaro, C, Sbarbati, A, Cigolini, M, Vogel, P, Ricquier, D & Fakan, S (1989b) Immunoelectron microscopical identification of the uncoupling protein in brown adipose tissue mitochondria. Biology of the Cell 67, 359362.Google Scholar
Cousin, B, Casteilla, L, Dani, C, Muzzin, P, Revelli, J-P, & Penicaud, L (1993) Adipose tissue from various anatomical size are characterized by different patterns of gene expression and regulation. Biochemical Journal 292, 873876.CrossRefGoogle Scholar
Cousin, B, Cinti, S, Morroni, M, Raimbault, S, Ricquier, D, Penicaud, L & Casteilla, L (1992) Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. Journal of Cell Science 103, 931942.Google Scholar
Crandall, DL, Hausman, GJ & Kral, JG (1997) A review of the microcirculation of adipose tissue: anatomic, metabolic and angiogenic perspectives. Microcirculation 4, 211232.CrossRefGoogle ScholarPubMed
De Matteis, R & Cinti, S (1998) Ultrastructural immunolocalisation of leptin receptor in mouse brain. Neuroendocrinology 68, 412419.Google Scholar
De Matteis, R, Dashtipour, K, Ognibene, A & Cinti, S (1998a) Localization of leptin receptor splice variants in mouse peripheral tissues by immunohistochemistry. Proceedings of the Nutrition Society 57, 441448.Google Scholar
De Matteis, R, Ricquier, D & Cinti, S (1998b) TH-, NPY-, SP-, and CGRP-immunoreactive nerves in interscapular brown adipose tissue of adult rats acclimated at different temperatures: an immunohistochemical study. Journal of Neurocytology 27, 877886.Google Scholar
Fawcett, DW (1952) A comparison of the histological organization and histochemical reactions of brown fat and ordinary fat. Journal of Morphology 90, 363372.CrossRefGoogle Scholar
Fleury, C, Neverova, M, Collins, S, Raimbault, S, Champigny, O, Levi-Meyrueis, C, Bouillaud, F, Seldin, MF, Surwit, RS, Ricquier, D & Warden, CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nature Genetics 15, 269272.Google Scholar
Flier, JS (1995) The adipocyte: storage depot or node on the energy information superhighway. Cell 80, 1518.CrossRefGoogle ScholarPubMed
Frederich, RC, Lollmann, B, Hamann, A, Napolitano-Rosen, A, Kahan, BB, Lowell, BB & Flier, JS (1995) Expression of the ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. Journal of Clinical Investigation 96, 16581663.CrossRefGoogle ScholarPubMed
Geloen, A, Collet, AJ & Bukowiecki, LJ (1992) Role of sympathetic innervation in brown adipocyte proliferation. American Journal of Physiology 263, R1176R1181.Google ScholarPubMed
Giacobino, J-P (1995) Beta3 adrenoceptor: an update. European Journal of Endocrinology 132, 377385.CrossRefGoogle Scholar
Gibson, SJ, Polak, JM, Bloom, SR, Sabate, IM, Mulderry, PM, Ghatei, MA, McGregor, GP, Morrison, JEB, Kelly, JS, Evans, RM & Rosenfeld, MG (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and eight other species. Journal of Neuroscience 4, 31013111.CrossRefGoogle ScholarPubMed
Giordano, A, Morroni, M, Carle, F, Gesuita, R, Marchesi, GF & Cinti, S (1998) Sensory nerves affect the recruitment and differentiation of rat periovarian brown adipocytes during cold acclimation. Journal of Cell Science 111, 25872594.CrossRefGoogle ScholarPubMed
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, 125136.Google Scholar
Giordano, A, Nisoli, E, Tonello, C, Cancello, R, Carruba, MO & Cinti, S (2000) Expression and distribution of heme oxygenase-1 and -2 in rat brown adipose tissue: the modulatory role of the noradrenergic system. FEBS Letters 487, 171175.CrossRefGoogle ScholarPubMed
Girardier, L & Stock, MJ (1983) Mammalian Thermogenesis. London: Chapman and Hall.Google Scholar
Himms-Hagen, J (1979) Obesity may be due to malfunctioning of brown fat. Canadian Medical Association Journal 121, 13611364.Google ScholarPubMed
Himms-Hagen, J, Melnyk, A, Zingaretti, MC, Ceresi, E, Barbatelli, G & Cinti, S (2000) Multilocular adipocytes in white adipose tissue of CL316,243-treated rats derive directly from white adipocytes. American Journal of Physiology 279, C670C681.Google Scholar
Holzer, P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24, 739768.CrossRefGoogle ScholarPubMed
Hsu, SM, Raine, L & Fanger, H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP procedures). Journal of Histochemistry and Cytochemistry 29, 577580.CrossRefGoogle ScholarPubMed
Klaus, S, Cassard-Doulcier, AM & Ricquier, D (1991a) Development of Phodopus sungorus brown preadipocytes in primary cell cultures: effect of an atypical beta-adrenergic agonist, insulin, and triiodothyronine on differentiation, mitochondrial development, and expression of the uncoupling protein UCP. Journal of Cell Biology 115, 17831790.Google Scholar
Klaus, S, Casteilla, L, Bouillaud, F & Ricquier, D (1991b) The uncoupling protein UCP: a membraneous mitochondrial ion carrier exclusively expressed in brown adipose tissue. International Journal of Biochemistry 23, 791801.CrossRefGoogle ScholarPubMed
Lafontan, M & Berlan, M (1993) Fat cells adrenergic receptors and the control of white and brown fat cells functions. Journal of Lipid Research 34, 10571091.CrossRefGoogle Scholar
Lee, Y, Kaway, Y, Shiosaka, S, Takami, K, Kiyama, H, Hylliard, C, McIntyre, I, Emson, PC & Tohyama, M (1986) Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: Immunohistochemical analysis. Brain Research 330, 194196.Google Scholar
Loncar, D (1991) Convertible adipose tissue in mice. Cell and Tissue Research 266, 149161.Google Scholar
Lowell, BB, Susulic, VS, Haman, A, Lawitts, JA, Himms-Hagen, J, Boyer, BB, Kozak, L & Flier, JS (1993) Development of morbid obesity in transgenic mice following the genetic ablation of brown adipose tissue. Nature 366, 740742.CrossRefGoogle 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 mRNA in mice with lesions of the hypothalamus and with mutations at the db locus. Proceedings of the National Academy of Sciences USA 929, 69576960.Google Scholar
Moncada, S & Higgs, A (1993) The L-arginine-nitric oxide pathway. New England Journal of Medicine 329, 20022012.Google Scholar
Morroni, M, Barbatelli, G, Zingaretti, MC & Cinti, S (1995) Immunohistochemical, ultrastructural and morphometric evidence for brown adipose tissue recruitment due to cold acclimation in old rats. International Journal of Obesity 19, 126131.Google Scholar
Nisoli, E, Tonello, C, Briscini, L & Carruba, M (1997) Inducible nitric oxide synthase in rat brown adipocytes: implications for blood flow to brown adipose tissue. Endocrinology 1387, 676682.CrossRefGoogle Scholar
Nnodim, JO & Lever, JD (1988) Neural and vascular provisions of rat interscapular brown adipose tissue. American Journal of Anatomy 182, 283293.CrossRefGoogle ScholarPubMed
Norman, D, Mukherjee, S, Symons, D, Jung, RT & Lever, JD (1988) Neuropeptides in interscapular and perirenal brown adipose tissue in the rat: a plurality of innervation. Journal of Neurocytology 17, 305311.CrossRefGoogle Scholar
Rehnmark, S, Kopecky, J, Jacobsson, A, Nechad, M, Herron, D, Nelson, BD, Obregon, MJ, Nedergaard, J & Cannon, B (1989) Brown adipocytes differentiated in vitro can express the gene for the uncoupling protein themogenin: effects of hypothyroidism and norepinephrine. Experimental Cell Research 182, 7583.CrossRefGoogle ScholarPubMed
Rothwell, NJ & Stock, MJ (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281, 3135.CrossRefGoogle ScholarPubMed
Sbarbati, A, Morroni, M, Zancanaro, C & Cinti, S (1991) Rat interscapular brown adipose tissue at different ages: a morphometric study. International Journal of Obesity 15, 581588.Google Scholar
Sbarbati, A, Zancanaro, C, Cigolini, M & Cinti, S (1987) Brown adipose tissue: a scanning electron microscopy study of tissue and cultured adipocytes. Acta Anatomica 128, 8488.Google Scholar
Schneider-Picard, G, Carpentier, JL & Orci, L (1980) Quantitative evaluation of gap junctions during development of the brown adipose tissue. Journal of Lipid Research 21, 600607.Google Scholar
Skofitsch, F & Jacobowitz, DM (1985) Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 6, 747754.Google Scholar
Terenghi, G, Polak, JM, Ghatei, MA, Mulderry, PK, Butler, JM, Unger, WG & Bloom, SR (1985) Distribution and origin of CGRP-immunoreactivity in the sensory innervation of the mammalian eye. Journal of Comparative Neurology 233, 505516.Google Scholar
Trayhurn, P & Nicholls, DG (1986) Brown Adipose Tissue. London: Edward Arnold.Google ScholarPubMed
Wells, HG (1940) Adipose tissue: a neglected subject. Journal of the American Medical Association 114, 21772183.Google Scholar
Young, P, Arch, JRS & Ashwell, M (1984) Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Letters 167, 1014.CrossRefGoogle ScholarPubMed
Zhang, Y, Proenea, R, Maffei, M, Barone, M, Leopold, L & Friedman, JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425432.Google Scholar