Adipose tissue resting energy expenditure and expression of genes involved in mitochondrial function are higher in women than in men

Journal of Clinical Endocrinology and Metabolism

Volumn 98, Issue 2, 2013, Pages

  Nookaew, Intawat ^a   Svensson, Per Arne ^b,e   Jacobson, Peter ^b   Margareta Jernas ^b   Taube, Magdalena ^b   Larsson, Ingrid ^b   Andersson Assarsson, Johanna C ^b,c   Sjöström, Lars ^b   Froguel, Philippe ^c,d   Walley, Andrew ^c   Nielsen, Jens ^a   Carlsson, Lena M S ^b  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^c HAMMERSMITH HOSPITAL   (United Kingdom)

^d CNRS   (France)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TESTOSTERONE; UNCOUPLING PROTEIN 1;

ADIPOSE TISSUE; ADULT; AGED; ANTHROPOMETRIC PARAMETERS; ARTICLE; BODY COMPOSITION; BODY FAT DISTRIBUTION; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ESTRADIOL BLOOD LEVEL; FAT MASS; FEMALE; FREE FAT MASS; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HOMEOSTASIS MODEL ASSESSMENT INSULIN RESISTANCE; HUMAN; HUMAN TISSUE; INSULIN SENSITIVITY; MAJOR CLINICAL STUDY; MALE; METABOLIC PARAMETERS; MITOCHONDRIAL GENE; MITOCHONDRIAL RESPIRATION; NUCLEOTIDE SEQUENCE; OBESITY; OXPHOS CR GENE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA GENE; PRIORITY JOURNAL; RESTING ENERGY EXPENDITURE; RESTING METABOLIC RATE; SEX DIFFERENCE; SUBCUTANEOUS FAT; TESTOSTERONE BLOOD LEVEL; UNCOUPLING PROTEIN 1 GENE; WAIST CIRCUMFERENCE; WAIST HIP RATIO; WEIGHT REDUCTION;

ADIPOCYTES, BROWN; ADIPOSE TISSUE; ADULT; AGED; BASAL METABOLISM; CROSS-SECTIONAL STUDIES; ENERGY METABOLISM; FEMALE; HUMANS; LIVER; MALE; MIDDLE AGED; MITOCHONDRIA; MUSCLE, SKELETAL; SEX CHARACTERISTICS;

EID: 84873669045     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2012-2764     Document Type: Article

References (40)

1. Smith SR, Lovejoy JC, Greenway F, et al. Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism. 2001;50(4):425-435.
2. Lemieux S, Prud'homme D, Bouchard C, Tremblay A, Despres JP. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr. 1993;58(4):463-467.
3. Bergman RN, Kim SP, Hsu IR, et al. Abdominal obesity: role in the pathophysiology of metabolic disease and cardiovascular risk. AmJ Med. 2007;120(2 suppl 1):S3-S8; discussion S29-S32.
4. Mathieu P, Poirier P, Pibarot P, Lemieux I, Despres JP. Visceral obesity: the link among inflammation, hypertension, and cardiovascular disease. Hypertension. 2009;53(4):577-584.
5. Tarnopolsky MA. Sex differences in exercise metabolism and the role of 17-β estradiol. Med Sci Sports Exerc. 2008;40(4):648-654.
6. Lofgren P, Hoffstedt J, Ryden M, et al. Major gender differences in the lipolytic capacity of abdominal subcutaneous fat cells in obesity observed before and after long-term weight reduction. J Clin Endocrinol Metab. 2002;87(2):764-771.
7. Kolehmainen M, Vidal H, Ohisalo JJ, Pirinen E, Alhava E, Uusitupa MI. Hormone sensitive lipase expression and adipose tissue metabolism show gender difference in obese subjects after weight loss. Int J Obes Relat Metab Disord. 2002;26(1):6 -16.
8. Montague CT, Prins JB, Sanders L, Digby JE, O'Rahilly S. Depotand sex-specific differences in human leptin mRNA expression: implications for the control of regional fat distribution. Diabetes. 1997;46(3):342-347.
9. Kern PA, Di Gregorio GB, Lu T, Rassouli N, Ranganathan G. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes. 2003;52(7):1779-1785.
10. Gallagher D, Belmonte D, Deurenberg P, et al. Organ-tissue mass measurement allows modeling of REE and metabolically active tissue mass. Am J Physiol. 1998;275(2 Pt 1):E249-E258.
11. Carlsson LM, Jacobson P, Walley A, et al. ALK7 expression is specific for adipose tissue, reduced in obesity and correlates to factors implicated in metabolic disease. Biochem Biophys Res Commun. 2009;382(2):309-314.
12. Larsson I, Lindroos AK, Peltonen M, Sjostrom L. Potassium per kilogram fat-free mass and total body potassium: predictions from sex, age, and anthropometry. Am J Physiol Endocrinol Metab. 2003;284(2):E416-E423.
13. Gummesson A, Jernas M, Svensson PA, et al. Relations of adipose tissue CIDEA gene expression to basal metabolic rate, energy restriction, and obesity: population-based and dietary intervention studies. J Clin Endocrinol Metab. 2007;92(12):4759-4765.
14. Svensson PA, Jernas M, Sjoholm K, et al. Gene expression in human brown adipose tissue. Int J Mol Med. 2011;27(2):227-232.
15. Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249-264.
16. Emilsson V, Thorleifsson G, Zhang B, et al. Genetics of gene expression and its effect on disease. Nature. 2008;452(7186):423-428.
17. Welle S, Tawil R, Thornton CA. Sex-related differences in gene expression in human skeletal muscle. PLoS One. 2008;3(1):e1385.
18. Schadt EE, Molony C, Chudin E, et al. Mapping the genetic architecture of gene expression in human liver. PLoS Biol. 2008;6(5): e107.
19. Patil KR, Nielsen J. Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci USA. 2005;102(8):2685-2689.
20. Oliveira AP, Patil KR, Nielsen J. Architecture of transcriptional regulatory circuits is knitted over the topology of bio-molecular interaction networks. BMC Syst Biol. 2008;2:17.
21. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article 3.
22. Benjamini Y, Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodological. 1995;57(1):289-300.
23. Alter O, Brown PO, Botstein D. Singular value decomposition for genome-wide expression data processing and modeling. Proc Natl Acad Sci USA. 2000;97(18):10101-10106.
24. Mootha VK, Lindgren CM, Eriksson KF, et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267-273.
25. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277-359.
26. Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360(15):1518-1525.
27. Muller MJ, Bosy-Westphal A, Kutzner D, Heller M. Metabolically active components of fat-free mass and resting energy expenditure in humans: recent lessons from imaging technologies. Obes Rev. 2002;3(2):113-122.
28. Weyer C, Snitker S, Rising R, Bogardus C, Ravussin E. Determinants of energy expenditure and fuel utilization in man: effects of body composition, age, sex, ethnicity and glucose tolerance in 916 subjects. Int J Obes Relat Metab Disord. 1999;23(7):715-722.
29. Johnstone AM, Murison SD, Duncan JS, Rance KA, Speakman JR. Factors influencing variation in basal metabolic rate include fat-free mass, fat mass, age, and circulating thyroxine but not sex, circulating leptin, or triiodothyronine. Am J Clin Nutr. 2005;82(5):941-948.
30. Geer EB, Shen W. Gender differences in insulin resistance, body composition, and energy balance. Gend Med. 2009;6(Suppl 1): 60-75.
31. Buchholz AC, Rafii M, Pencharz PB. Is resting metabolic rate different between men and women? Br J Nutr. 2001;86(6):641-646.
32. Van Gaal LF, Vansant GA, De Leeuw IH. Factors determining energy expenditure during very-low-calorie diets. Am J Clin Nutr. 1992;56(1 suppl):224S-229S.
33. Wu Z, Puigserver P, Andersson U, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115-124.
34. Wallace DC, Fan W, Procaccio V. Mitochondrial energetics and therapeutics. Annu Rev Pathol. 5:297-348.
35. Heaton JM. The distribution of brown adipose tissue in the human. J Anat. 1972;112(Pt 1):35-39.
36. Zingaretti MC, Crosta F, Vitali A, et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009; 23(9):3113-3120.
37. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293(2):E444-E452.
38. Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. NEngl J Med. 2009; 360(15):1509-1517.
39. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360(15):1500-1508.
40. Rodriguez-Cuenca S, Pujol E, Justo R, et al. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem. 2002; 277(45):42958-42963.