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      Sex matters: The effects of biological sex on adipose tissue biology and energy metabolism

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          Abstract

          Adipose tissue is a complex and multi-faceted organ. It responds dynamically to internal and external stimuli, depending on the developmental stage and activity of the organism. The most common functional subunits of adipose tissue, white and brown adipocytes, regulate and respond to endocrine processes, which then determine metabolic rate as well as adipose tissue functions. While the molecular aspects of white and brown adipose biology have become clearer in the recent past, much less is known about sex-specific differences in regulation and deposition of adipose tissue, and the specific role of the so-called pink adipocytes during lactation in females. This review summarises the current understanding of adipose tissue dynamics with a focus on sex-specific differences in adipose tissue energy metabolism and endocrine functions, focussing on mammalian model organisms as well as human-derived data. In females, pink adipocytes trans-differentiate during pregnancy from subcutaneous white adipocytes and are responsible for milk-secretion in mammary glands. Overlooking biological sex variation may ultimately hamper clinical treatments of many aspects of metabolic disorders.

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          Highlights

          • •

            Sex differences of endocrine and metabolic function in adipose tissue.

          • •

            Sex-specific differences in regulation and deposition of fat are often overlooked.

          • •

            Pink adipocytes trans-differentiate from white fat cells in pregnant females.

          • •

            Gender-specific medicine: implication for therapeutic approaches in metabolic disease.

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          Most cited references79

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          FAT SIGNALS - Lipases and Lipolysis in Lipid Metabolism and Signaling

          Rudolf Zechner, Robert Zimmermann, Thomas O. Eichmann … (2012)
          Lipolysis is defined as the catabolism of triacylglycerols stored in cellular lipid droplets. Recent discoveries of essential lipolytic enzymes and characterization of numerous regulatory proteins and mechanisms have fundamentally changed our perception of lipolysis and its impact on cellular metabolism. New findings that lipolytic products and intermediates participate in cellular signaling processes and that “lipolytic signaling” is particularly important in many nonadipose tissues unveil a previously underappreciated aspect of lipolysis, which may be relevant for human disease.
          Article 0 comments Cited 381 times – based on 0 reviews     Review now
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            In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding.

            Yun-Hee Lee, Anelia P Petkova, Emilio Mottillo … (2012)
            Nutritional and pharmacological stimuli can dramatically alter the cellular phenotypes in white adipose tissue (WAT). Utilizing genetic lineage tracing techniques, we demonstrate that brown adipocytes (BA) that are induced by β3-adrenergic receptor activation in abdominal WAT arise from the proliferation and differentiation of cells expressing platelet-derived growth factor receptor alpha (PDGFRα), CD34, and Sca-1 (PDGFRα(+) cells). PDGFRα(+) cells have a unique morphology in which extended processes contact multiple cells in the tissue microenvironment. Surprisingly, these cells also give rise to white adipocytes (WA) that can comprise up to 25% of total fat cells in abdominal fat pads following 8 weeks of high-fat feeding. Isolated PDGFRα(+) cells differentiated into both BA and WA in vitro and generated WA after transplantation in vivo. The identification of PDGFRα(+) cells as bipotential adipocyte progenitors will enable further investigation of mechanisms that promote therapeutic cellular remodeling in adult WAT. Copyright © 2012 Elsevier Inc. All rights reserved.
            Article 0 comments Cited 260 times – based on 0 reviews     Review now
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              Nonshivering thermogenesis and its adequate measurement in metabolic studies.

              Barbara Cannon, Jan Nedergaard (2011)
              Alterations in nonshivering thermogenesis are presently discussed as being both potentially causative of and able to counteract obesity. However, the necessity for mammals to defend their body temperature means that the ambient temperature profoundly affects the outcome and interpretation of metabolic experiments. An adequate understanding and assessment of nonshivering thermogenesis is therefore paramount for metabolic studies. Classical nonshivering thermogenesis is facultative, i.e. it is only activated when an animal acutely requires extra heat (switched on in minutes), and adaptive, i.e. it takes weeks for an increase in capacity to develop. Nonshivering thermogenesis is fully due to brown adipose tissue activity; adaptation corresponds to the recruitment of this tissue. Diet-induced thermogenesis is probably also facultative and adaptive and due to brown adipose tissue activity. Although all mammals respond to injected/infused norepinephrine (noradrenaline) with an increase in metabolism, in non-adapted mammals this increase mainly represents the response of organs not involved in nonshivering thermogenesis; only the increase after adaptation represents nonshivering thermogenesis. Thermogenesis (metabolism) should be expressed per animal, and not per body mass [not even to any power (0.75 or 0.66)]. A 'cold tolerance test' does not examine nonshivering thermogenesis capacity; rather it tests shivering capacity and endurance. For mice, normal animal house temperatures are markedly below thermoneutrality, and the mice therefore have a metabolic rate and food consumption about 1.5 times higher than their intrinsic requirements. Housing and examining mice at normal house temperatures carries a high risk of identifying false positives for intrinsic metabolic changes; in particular, mutations/treatments that affect the animal's insulation (fur, skin) may lead to such problems. Correspondingly, true alterations in intrinsic metabolic rate remain undetected when metabolism is examined at temperatures below thermoneutrality. Thus, experiments with animals kept and examined at thermoneutrality are likely to yield an improved possibility of identifying agents and genes important for human energy balance.
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                Author and article information

                Contributors
                Teresa G. Valencak
                Anne Osterrieder
                Tim J. Schulz
                Journal
                Journal ID (nlm-ta): Redox Biol
                Journal ID (iso-abbrev): Redox Biol
                Title: Redox Biology
                Publisher: Elsevier
                ISSN (Electronic): 2213-2317
                Publication date PMC-release: 13 April 2017
                Publication date Collection: August 2017
                Publication date (Electronic): 13 April 2017
                Volume: 12
                Pages: 806-813
                Affiliations
                [a ]Institute of Physiology, Pathophysiology and Biophysics, Department of Biomedical Sciences, University of Veterinary Medicine Vienna, Veterinärplatz 1, A-1210 Vienna, Austria
                [b ]Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Gipsy Lane, Headington, Oxford OX3 0BP, UK
                [c ]Department of Adipocyte Development and Nutrition, German Institute of Human Nutrition Potsdam-Rehbrücke, 114-116, Arthur-Scheunert-Allee, 14558 Nuthetal, Germany
                [d ]German Center for Diabetes Research (DZD), 85764 München-Neuherberg, Germany
                Author notes
                Article
                Publisher ID: S2213-2317(17)30234-3
                DOI: 10.1016/j.redox.2017.04.012
                PMC ID: 5406544
                PubMed ID: 28441629
                SO-VID: 5293bd40-7f4a-4854-9895-eab8b3dab4c5
                Copyright © Crown Copyright © 2017 Published by Elsevier B.V.
                License:

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 29 March 2017
                Date accepted : 8 April 2017
                Categories
                Subject: Review Article

                Keywords: body fatness,adipose tissue,sex-specific differences,adipokines,adipocytes,obesity,energy metabolism
                Data availability:
                Keywords: body fatness, adipose tissue, sex-specific differences, adipokines, adipocytes, obesity, energy metabolism

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