Recent advances in the adaptations of adipose tissue to physical activity: Morphology and adipose tissue cellularity

White adipose tissue (WAT) is located beneath the skin as subcutaneous adipose tissue (SAT), around internal organs as visceral adipose tissue (VAT), pericardial and epicardial adipose tissue, and inside muscles in human beings. Recent studies indicate that developmental and patterning genes are differentially expressed in SAT and VAT, and some of these genes exhibit changes in expression that closely correlate with the extent of obesity and pattern of fat distribution. Furthermore, the development of adipocytes from mesenchymal stem/progenitor cells is thought to be mediated by developmental signaling molecules including nodal, Wnt/ wingless (Wg), bone morphogenetic proteins (BMPs), fibroblast growth factors (FGF), and others. Of these, BMPs and the FGF family have been suggested to play a role in maintaining energy homeostasis. However, it remains unclear whether these developmental and patterning genes are associated with morphological changes in WAT in response to exercise training (TR). On the other hand, when TR reduces the number of adipocytes in WAT, it increases preadipocyte factor 1 mRNA expression but down-regulates peroxisome proliferator-activated receptor-γ mRNA expression in stromal-vascular fraction cells, including adipose tissuederived stromal cells, via the up-regulation of hypoxia-inducible factor-1α, which may also upregulate the mRNA expression of vascular endothelial growth factor-A and its receptor. The purpose of this review is to summarize the research to date on the morphology of WAT and adipose tissue cellularity in exercise adaptation.

[1]  T. Kizaki,et al.  Effect of physical exercise on lipolysis in white adipocytes , 2012 .

[2]  T. Kizaki,et al.  The effects of exercise on macrophage function , 2012 .

[3]  T. Kizaki,et al.  Effect of exercise training on the density of endothelial cells in the white adipose tissue of rats , 2011, Scandinavian journal of medicine & science in sports.

[4]  E. Maratos-Flier,et al.  Fibroblast growth factor 21 is a metabolic regulator that plays a role in the adaptation to ketosis. , 2011, The American journal of clinical nutrition.

[5]  C. Ugrinowitsch,et al.  Effect of different resistance-training regimens on the WNT-signaling pathway , 2011, European Journal of Applied Physiology.

[6]  M. Stumvoll,et al.  Genetic and Evolutionary Analyses of the Human Bone Morphogenetic Protein Receptor 2 (BMPR2) in the Pathophysiology of Obesity , 2011, PloS one.

[7]  T. Kizaki,et al.  Effects of exercise training on adipogenesis of stromal-vascular fraction cells in rat epididymal white adipose tissue. , 2010, Acta physiologica.

[8]  E. Arner,et al.  Regional impact of adipose tissue morphology on the metabolic profile in morbid obesity , 2010, Diabetologia.

[9]  J. Flier,et al.  Obesity Is a Fibroblast Growth Factor 21 (FGF21)-Resistant State , 2010, Diabetes.

[10]  Qing Yang,et al.  Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK–SIRT1–PGC-1α pathway , 2010, Proceedings of the National Academy of Sciences.

[11]  T. Kizaki,et al.  Effect of exercise training on adipocyte-size-dependent expression of leptin and adiponectin. , 2010, Life sciences.

[12]  J. Jarolimova,et al.  Gbb/BMP signaling is required to maintain energy homeostasis in Drosophila. , 2010, Developmental biology.

[13]  A. VanHook.  BMPing Up Metabolism , 2010, Science Signaling.

[14]  S. Bernard,et al.  Adipocyte Turnover: Relevance to Human Adipose Tissue Morphology , 2009, Diabetes.

[15]  T. Schulz,et al.  Emerging role of bone morphogenetic proteins in adipogenesis and energy metabolism. , 2009, Cytokine & growth factor reviews.

[16]  M. Matoulek,et al.  Serum concentrations and tissue expression of a novel endocrine regulator fibroblast growth factor‐21 in patients with type 2 diabetes and obesity , 2009, Clinical endocrinology.

[17]  E. Hoffman,et al.  Differences in fat and muscle mass associated with a functional human polymorphism in a post‐transcriptional BMP2 gene regulatory element , 2009, Journal of cellular biochemistry.

[18]  H. Aburatani,et al.  COUP-TFII acts downstream of Wnt/β-catenin signal to silence PPARγ gene expression and repress adipogenesis , 2009, Proceedings of the National Academy of Sciences.

[19]  Antonio Vidal-Puig,et al.  Adipogenesis and WNT signalling , 2009, Trends in Endocrinology & Metabolism.

[20]  K. Chamari,et al.  Review on leptin and adiponectin responses and adaptations to acute and chronic exercise , 2008, British Journal of Sports Medicine.

[21]  C. Kahn,et al.  New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure , 2008, Nature.

[22]  Wei Zheng,et al.  Differential effects of cyclic and static stretch on coronary microvascular endothelial cell receptors and vasculogenic/angiogenic responses. , 2008, American journal of physiology. Heart and circulatory physiology.

[23]  Tom Britton,et al.  Dynamics of fat cell turnover in humans , 2008, Nature.

[24]  B. Nicklas,et al.  Effects of exercise on adipokines and the metabolic syndrome , 2008, Current diabetes reports.

[25]  O. MacDougald,et al.  Wnt/β-catenin signaling in adipogenesis and metabolism , 2007 .

[26]  C. Kahn,et al.  Developmental Origin of Fat: Tracking Obesity to Its Source , 2007, Cell.

[27]  M. Longaker,et al.  Hypoxia inducible factor-1alpha deficiency affects chondrogenesis of adipose-derived adult stromal cells. , 2007, Tissue engineering.

[28]  C. Herder,et al.  Relationship between adipocyte size and adipokine expression and secretion. , 2007, The Journal of clinical endocrinology and metabolism.

[29]  M. Shibuya.  Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. , 2006, Journal of biochemistry and molecular biology.

[30]  C. Kahn,et al.  Evidence for a role of developmental genes in the origin of obesity and body fat distribution. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[31]  David M. Umulis,et al.  Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing , 2005, Development.

[32]  M. Hedrick,et al.  Multipotential differentiation of adipose tissue-derived stem cells. , 2005, The Keio journal of medicine.

[33]  Zhen Yan,et al.  Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. , 2005, Biochemical and biophysical research communications.

[34]  A. Kispert,et al.  The T-box transcription factor Tbx15 is required for skeletal development , 2005, Mechanisms of Development.

[35]  Di Chen,et al.  Bone Morphogenetic Proteins , 2004, Growth factors.

[36]  T. Hudson,et al.  A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. , 2004, Obesity research.

[37]  P. Favrel,et al.  Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. , 2004, Developmental and comparative immunology.

[38]  J. Helge,et al.  Interstitial glycerol concentrations in human skeletal muscle and adipose tissue during graded exercise. , 2004, Acta physiologica Scandinavica.

[39]  B. Stallknecht.  Influence of physical training on adipose tissue metabolism--with special focus on effects of insulin and epinephrine. , 2004, Danish medical bulletin.

[40]  S. Egginton,et al.  Differential expression of Flk-1 and Flt-1 in rat skeletal muscle in response to chronic ischaemia: favourable effect of muscle activity. , 2003, Clinical science.

[41]  M. Cantile,et al.  HOX gene network is involved in the transcriptional regulation of in vivo human adipogenesis , 2003, Journal of cellular physiology.

[42]  Min Zhu,et al.  Human adipose tissue is a source of multipotent stem cells. , 2002, Molecular biology of the cell.

[43]  G. David,et al.  Developmental roles of the glypicans. , 2001, Seminars in cell & developmental biology.

[44]  H. Lorenz,et al.  Multilineage cells from human adipose tissue: implications for cell-based therapies. , 2001, Tissue engineering.

[45]  J. Fluckey,et al.  Effect of exercise training on in vivo lipolysis in intra-abdominal adipose tissue in rats. , 2000, American journal of physiology. Endocrinology and metabolism.

[46]  J. Bülow,et al.  Effect of training on insulin sensitivity of glucose uptake and lipolysis in human adipose tissue. , 2000, American journal of physiology. Endocrinology and metabolism.

[47]  Robert Ross,et al.  Reduction in Obesity and Related Comorbid Conditions after Diet-Induced Weight Loss or Exercise-Induced Weight Loss in Men , 2000, Annals of Internal Medicine.

[48]  G. Neufeld,et al.  Vascular endothelial growth factor (VEGF) and its receptors , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[49]  H. Sul,et al.  Transcriptional Control of the pref-1 Gene in 3T3-L1 Adipocyte Differentiation , 1998, The Journal of Biological Chemistry.

[50]  M. Gessler,et al.  Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family , 1998, Mechanisms of Development.

[51]  G. Semenza,et al.  Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1 , 1996, Molecular and cellular biology.

[52]  J. Bülow,et al.  Effect of training on epinephrine-stimulated lipolysis determined by microdialysis in human adipose tissue. , 1995, The American journal of physiology.

[53]  M. Tsai,et al.  Chicken ovalbumin upstream promoter transcription factor (COUP-TF): Expression during mouse embryogenesis , 1995, The Journal of Steroid Biochemistry and Molecular Biology.

[54]  H. Sul,et al.  Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation , 1993, Cell.

[55]  A. Joyner,et al.  En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. , 1987, Genes & development.

[56]  J. Hirsch,et al.  Adipose tissue cellularity in human obesity. , 1976, Clinics in endocrinology and metabolism.

[57]  L. Sjöström,et al.  Regional adipose tissue cellularity in relation to metabolism in young and middle-aged women. , 1975, Metabolism: clinical and experimental.

[58]  J. Hirsch,et al.  Cellularity of adipose depots in the genetically obese Zucker rat. , 1971, Journal of lipid research.

[59]  F. Karpe,et al.  Physical activity and exercise in the regulation of human adipose tissue physiology. , 2012, Physiological reviews.

[60]  T. He,et al.  Bone Morphogenetic Proteins and Adipocyte Differentiation , 2007 .

[61]  N. Gerry,et al.  Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. , 2007, American journal of physiology. Endocrinology and metabolism.

[62]  O. MacDougald,et al.  Wnt/beta-catenin signaling in adipogenesis and metabolism. , 2007, Current Opinion in Cell Biology.

[63]  肥田 綾,et al.  Serum bFGF levels are reduced in Japanese overweight men and restored by a 6-month exercise education , 2006 .

[64]  J. Fluckey,et al.  Effect of exercise training on in vivo insulin-stimulated glucose uptake in intra-abdominal adipose tissue in rats. , 2000, American journal of physiology. Endocrinology and metabolism.

[65]  J. Hirsch,et al.  Cellularity of rat adipose tissue: effects of growth, starvation, and obesity. , 1969, Journal of lipid research.