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Obesity modifies expression profiles of metabolic markers in superficial and deep subcutaneous abdominal adipose tissue depots

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Abstract

While visceral adipose tissue (VAT) associates to obesity, there is debate for subcutaneous adipose tissue (SAT). One explanation may be SAT subcompartments, superficial-SAT (sSAT) and deep-SAT (dSAT), recently recognized as independent depots. Our aim was to establish roles for sSAT/dSAT with obesity by examining the expression of proteins key to adipocyte metabolism. Paired biopsies from sSAT and dSAT of 10 normal-weight (BMI 21.8 ± 0.8 kg/m2) and 11 obese subjects (BMI 44 ± 2.1 kg/m2) were analyzed for differences in insulin sensitivity using adiponectin, GLUT4 and resistin, glucocorticoid metabolism by 11βHSD1 and alterations of the adipokines leptin and TNFα. Between lean and obese subjects, sSAT and dSAT changes for GLUT4, resistin and TNFα were equivalent. Resistin and TNFα increased in both obese SAT sub-compartments; 33-fold (sSAT; P < 0.006) and 18.5-fold (dSAT; P < 0.003) higher resistin, with undetectable in leans to significant TNFα levels in obese. In contrast, GLUT4 showed 5.5-fold (sSAT; P < 0.03) and 7-fold (dSAT; P < 0.03) lower levels in obese, correlating to BMI (r = −0.6423, P = 0.007) and HOMA-IR (r = −0.5882, P = 0.017). Exclusive sSAT-specific differences were observed for adiponectin, leptin, and 11βHSD1. Both sSAT 11βHSD1 and leptin increased in obese, with 11βHSD1 2.5-fold (P = 0.052) and leptin 3.3-fold (P < 0.008) higher, with 11βHSD1 correlating to HOMA-IR (r = 0.5203, P = 0.0323) and leptin to BMI (r = 0.5810, P = 0.01). In contrast, obese had 7-fold (P < 0.02) lower sSAT adiponectin, correlating to BMI (r = −0.5178, P = 0.027) and HOMA-IR (r = −0.4570, P = 0.049). Overall, sSAT and dSAT are distinct abdominal adipose tissue depots with independent metabolic functions. Between the two, sSAT shows clear independent effects that associate to obesity and its metabolic complications.

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References

  1. J. Vague, The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout and uric calculous disease. Am. J. Clin. Nutr. 4, 20–31 (1956)

    CAS  PubMed  Google Scholar 

  2. B.L. Wajchenberg, Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr. Rev. 21, 697–738 (2000)

    Article  CAS  PubMed  Google Scholar 

  3. J.A. Nazare, J.D. Smith, A.L. Borel, S.M. Haffner, B. Balkau, R. Ross, C. Massien, N. Alméras, J.P. Després, Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the international study of prediction of intra-abdominal adiposity and its relationship with cardiometabolic risk/intra-abdominal adiposity. Am. J. Clin. Nutr. 96, 714–726 (2012)

    Article  CAS  PubMed  Google Scholar 

  4. M.J. Lee, Y. Wu, S.K. Fried, Adipose tissue heterogeneity: implication of depot differences in adipose tissue for obesity complications. Mol. Aspects Med. 34, 1–11 (2013)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. C. Maffeis, R. Manfredi, M. Trombetta, S. Sordelli, M. Storti, T. Benuzzi, R.C. Bonadonna, Insulin sensitivity is correlated with subcutaneous but not visceral body fat in overweight and obese prepubertal children. J. Clin. Endocrinol. Metab. 93, 2122–2128 (2008)

    Article  CAS  PubMed  Google Scholar 

  6. A.A. Bremer, S. Devaraj, A. Afify, I. Jialal, Adipose tissue dysregulation in patients with metabolic syndrome. J. Clin. Endocrinol. Metab. 96, E1782–E1788 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. A.A. Bremer, I. Jialal, Adipose tissue dysfunction in nascent metabolic syndrome. J. Obes. 2013, 393192 (2013). doi:10.1155/2013/393192

    Article  PubMed Central  PubMed  Google Scholar 

  8. H.G. Alexander, A.E. Dugdale, Fascial planes within subcutaneous fat in humans. Eur. J. Clin. Nutr. 46, 903–906 (1992)

    CAS  PubMed  Google Scholar 

  9. D.E. Kelley, F.L. Thaete, F. Troost, T. Huwe, B.H. Goodpaster, Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 278, E941–E948 (2000)

    CAS  PubMed  Google Scholar 

  10. G.E. Walker, B. Verti, P. Marzullo, G. Savia, M. Mencarelli, F. Zurleni, A. Liuzzi, A.M. Di Blasio, Deep sub-cutaneous adipose tissue (dSAT): a metabolically distinct abdominal adipose depot. Obes. Res. 15, 1933–1943 (2007)

    Article  CAS  Google Scholar 

  11. A. Roca-Rivada, J. Alonso, O. Al-Massadi, C. Castelao, J.R. Peinado, L.M. Seoane, F.F. Casanueva, M. Pardo, Secretome analysis of rat adipose tissues shows location-specific roles for each depot type. Proteomics 74, 1068–1079 (2011)

    Article  CAS  PubMed  Google Scholar 

  12. M. Pardo, A. Roca-Rivada, L.M. Seoane, F.F. Casanueva, Obesidomics: contribution of adipose tissue secretome analysis to obesity research. Endocrine 41, 374–383 (2012)

    Article  CAS  PubMed  Google Scholar 

  13. N. Garcia de la Torre, M.A. Rubio, E. Bordiú, L. Cabrerizo, E. Aparicio, C. Hernández, A. Sánchez-Pernaute, L. Díez-Valladares, A. Torres, M. Puente, A.L. Charro, Effects of weight loss after bariatric surgery for morbid obesity on vascular endothelial growth factor-A, adipocytokines, and insulin. J. Clin. Endocrinol. Metab. 93, 4276–4281 (2008)

    Article  CAS  PubMed  Google Scholar 

  14. Y. Matsuzawa, T. Funahashi, T. Nakamura, The concept of metabolic syndrome: contribution of visceral fat accumulation and its molecular mechanism. J. Atheroscler. Thromb. 18, 629–639 (2011)

    Article  CAS  PubMed  Google Scholar 

  15. E. Carvalho, K. Kotani, O.D. Peroni, B.B. Kahn, Adipose-specific overexpression of GLUT4 reverses insulin resistance and diabetes in mice lacking GLUT4 selectively in muscle. Am. J. Physiol. Endocrinol. Metab. 89, E551–E561 (2005)

    Article  Google Scholar 

  16. A. Marette, P. Mauriège, B. Marcotte, C. Atgié, C. Bouchard, G. Thériault, L.J. Bukowiecki, P. Marceau, S. Biron, A. Nadeau, J.P. Després, Regional variation in adipose tissue insulin action and GLUT4 glucose transporter expression in severely obese premenopausal women. Diabetologia 40, 590–598 (1997)

    Article  CAS  PubMed  Google Scholar 

  17. C.M. Steppan, S.T. Bailey, S. Bhat, E.J. Brown, R.R. Banerjee, C.M. Wright, H.R. Patel, R.S. Ahima, M.A. Lazar, The hormone resistin links obesity to diabetes. Nature 409, 292–293 (2001)

    Article  Google Scholar 

  18. R.Z. Yang, Q. Huang, A. Xu, J.C. McLenithan, J.A. Eisen, A.R. Shuldiner, S. Alkan, D.W. Gong, Comparative studies of resistin expression and phylogenomics in human and mouse. Biochem. Biophys. Res. Commun. 310, 927–935 (2003)

    Article  CAS  PubMed  Google Scholar 

  19. P.M. Stewart, J.W. Tomlinson, Cortisol, 11 beta-hydroxysteroid dehydrogenase type 1 and central obesity. Trends Endocrinol. Metab. 13, 94–96 (2002)

    Article  CAS  PubMed  Google Scholar 

  20. E.E. Kershaw, N.M. Morton, H. Dhillon, L. Ramage, J.R. Seckl, J.S. Flier, Adipocyte-specific glucocorticoid inactivation protects against diet-induced obesity. Diabetes 54, 1023–1031 (2005)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. N.M. Morton, J.M. Paterson, H. Masuzaki, M.C. Holmes, B. Staels, C. Fievet, B.R. Walker, J.S. Flier, J.J. Mullins, J.R. Seckl, Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11 beta-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53, 931–938 (2004)

    Article  CAS  PubMed  Google Scholar 

  22. M. Wamil, J.H. Battle, S. Turban, T. Kipari, D. Seguret, R. de Sousa Peixoto, Y.B. Nelson, D. Nowakowska, D. Ferenbach, L. Ramage, K.E. Chapman, J. Hughes, D.R. Dunbar, J.R. Seckl, N.M. Morton, Novel fat depot–specific mechanisms underlie resistance to visceral obesity and inflammation in 11β-hydroxysteroid dehydrogenase type 1–deficient mice. Diabetes 60, 1158–1167 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. M. Cnop, M.J. Landchild, J. Vidal, P.J. Havel, N.G. Knowles, D.R. Carr, F. Wang, R.L. Hull, E.J. Boyko, B.M. Retzlaff, C.E. Walden, R.H. Knopp, S.E. Kahn, The concurrent accumulation of intra-abdominal and subcutaneous fat explains the association between insulin resistance and plasma leptin concentrations : distinct metabolic effects of two fat compartments. Diabetes 51, 1005–1015 (2002)

    Article  CAS  PubMed  Google Scholar 

  24. Y.L. Cao, C.Z. Hu, X. Meng, D.F. Wang, J. Zhang, Expression of TNF-alpha protein in omental and subcutaneous adipose tissue in obesity. Diabetes Res. Clin. Pract. 79, 214–219 (2008)

    Article  CAS  PubMed  Google Scholar 

  25. H. Gottschling-Zeller, M. Birgel, D. Scriba, W.F. Blum, H. Hauner, Depot-specific release of leptin from subcutaneous and omental adipocytes in suspension culture: effect of tumor necrosis factor-alpha and transforming growth factor-beta1. Eur. J. Endocrinol. 141, 436–442 (1999)

    Article  CAS  PubMed  Google Scholar 

  26. A.S. Lihn, B. Richelsen, S.B. Pedersen, S.B. Haugaard, G.S. Rathje, S. Madsbad, O. Andersen, Increased expression of TNF-alpha, IL-6, and IL-8 in HALS: implications for reduced adiponectin expression and plasma levels. Am. J. Physiol. Endocrinol. Metab. 285, E1072–E1080 (2003)

    CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. Barbara Verti and Dr. Giulio Savia for their assistance and Professor Antonio Liuzzi for his exclusive support and mentorship.

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Correspondence to Gillian E. Walker.

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Walker, G.E., Marzullo, P., Prodam, F. et al. Obesity modifies expression profiles of metabolic markers in superficial and deep subcutaneous abdominal adipose tissue depots. Endocrine 46, 99–106 (2014). https://doi.org/10.1007/s12020-013-0040-x

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  • DOI: https://doi.org/10.1007/s12020-013-0040-x

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