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Published in: Endocrine 1/2019

01-07-2019 | Obesity | Original Article

Serum IGF-binding protein 2 (IGFBP-2) concentrations change early after gastric bypass bariatric surgery revealing a possible marker of leptin sensitivity in obese subjects

Authors: Giovanni Ceccarini, Caterina Pelosini, Federica Ferrari, Silvia Magno, Jacopo Vitti, Guido Salvetti, Carlo Moretto, Antonio Marioni, Piero Buccianti, Paolo Piaggi, Margherita Maffei, Ferruccio Santini

Published in: Endocrine | Issue 1/2019

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Abstract

Purpose

Expression of IGFBP-2 in mice is regulated by leptin. Over-expression of IGFBP-2 is associated with reduced caloric intake and resistance to weight gain. Hormonal variations contributing to weight loss occur very early after bariatric surgery but have not been fully elucidated. We evaluated IGFBP-2 serum changes after bariatric surgery and their relationship with leptin variations to test the hypothesis that an increase of leptin sensitivity may explain some of the effects of gastric bypass.

Methods

This is a historical prospective study. Fifty-one obese patients (41 women e 10 men), 9 non-obese surgical controls and 41 lean matched controls were studied. Serum IGFBP-2 and leptin were measured after bariatric bypass surgery at various time points up to 18 months, after non-bariatric laparoscopic surgery in a control group, and in lean matched controls.

Results

Compared to lean controls, serum IGFBP-2 levels were lower in obese patients. After gastric bypass, IGFBP-2 significantly increased at 3 days and became normal before the occurrence of relevant changes in body weight, remaining stable up to 18 months after surgery. IGFBP-2/leptin ratio increased early after surgery and became normal after one year.

Conclusions

After gastric bypass, serum IGFBP-2 increases in a window of time when variations of hormones mediating the effects of bariatric surgery occur. Our results suggest that IGFBP-2, a leptin-regulated protein, may be an in-vivo marker of leptin action. If this is the case, an early improvement of leptin sensitivity might contribute to the anorectic effect of gastric bypass.
Literature
1.
go back to reference S. Rajaram, D. Baylink, S. Mohan, Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr. Rev. 6, 801–831 (1997) S. Rajaram, D. Baylink, S. Mohan, Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr. Rev. 6, 801–831 (1997)
2.
go back to reference A. Hoeflich, V.C. Russo, Physiology and pathophysiology of IGFBP-1 and IGFBP-2 - consensus and dissent on metabolic control and malignant potential. Best. Pract. Res. Clin. Endocrinol. Metab. 5, 685–700 (2015)CrossRef A. Hoeflich, V.C. Russo, Physiology and pathophysiology of IGFBP-1 and IGFBP-2 - consensus and dissent on metabolic control and malignant potential. Best. Pract. Res. Clin. Endocrinol. Metab. 5, 685–700 (2015)CrossRef
3.
go back to reference X. Yao, S. Sun, X. Zhou, W. Guo, L. Zhang, IGF-binding protein 2 is a candidate target of therapeutic potential in cancer. Tumor Biol. 2, 1451–1459 (2016)CrossRef X. Yao, S. Sun, X. Zhou, W. Guo, L. Zhang, IGF-binding protein 2 is a candidate target of therapeutic potential in cancer. Tumor Biol. 2, 1451–1459 (2016)CrossRef
4.
go back to reference C.M. Boney, B.M. Moats Staats, A.D. Stiles, A.J. D’Ercole, Expression of insulin-like growth factor – 1 (IGF-I) and IGF- binding proteins during adipogenesis. Endocrinology 5, 1863–1868 (1994)CrossRef C.M. Boney, B.M. Moats Staats, A.D. Stiles, A.J. D’Ercole, Expression of insulin-like growth factor – 1 (IGF-I) and IGF- binding proteins during adipogenesis. Endocrinology 5, 1863–1868 (1994)CrossRef
5.
go back to reference Z. Li, F. Picard, Modulation of IGFBP-2 mRNA expression in white adipose tissue upon aging and obesity. Horm. Metab. Res. 11, 787–791 (2010)CrossRef Z. Li, F. Picard, Modulation of IGFBP-2 mRNA expression in white adipose tissue upon aging and obesity. Horm. Metab. Res. 11, 787–791 (2010)CrossRef
6.
go back to reference S.W. Yau, B.A. Henry, V.C. Russo, G.K. McConell, I.J. Clarke, G.A. Werther, M.A. Sabin, Leptin enhances insulin sensitivity by direct and sympathetic nervous system regulation of muscle IGFBP-2 expression: evidence from nonrodent models. Endocrinology 6, 2133–2143 (2014)CrossRef S.W. Yau, B.A. Henry, V.C. Russo, G.K. McConell, I.J. Clarke, G.A. Werther, M.A. Sabin, Leptin enhances insulin sensitivity by direct and sympathetic nervous system regulation of muscle IGFBP-2 expression: evidence from nonrodent models. Endocrinology 6, 2133–2143 (2014)CrossRef
7.
go back to reference G. Xi, M.A. Solum, C. Wai, L. Maile, C.J. Rosen, D.R. Clemmons, The heparin-binding domains of igfbp-2 mediate its inhibitory effect on preadipocyte differentiation and fat development in male mice. Endocrinology 11, 4146–4157 (2013)CrossRef G. Xi, M.A. Solum, C. Wai, L. Maile, C.J. Rosen, D.R. Clemmons, The heparin-binding domains of igfbp-2 mediate its inhibitory effect on preadipocyte differentiation and fat development in male mice. Endocrinology 11, 4146–4157 (2013)CrossRef
8.
go back to reference S.W. Yau, V.C. Russo, I.J. Clarke, F.R. Dunshea, G.A. Werther, M.A. Sabin, IGFBP-2 inhibits adipogenesis and lipogenesis in human visceral, but not subcutaneous, adipocytes. Int. J. Obes. 5, 770–781 (2015)CrossRef S.W. Yau, V.C. Russo, I.J. Clarke, F.R. Dunshea, G.A. Werther, M.A. Sabin, IGFBP-2 inhibits adipogenesis and lipogenesis in human visceral, but not subcutaneous, adipocytes. Int. J. Obes. 5, 770–781 (2015)CrossRef
9.
go back to reference S.B. Wheatcroft, M.T. Kearney, A.M. Shah, V.E. Ezzat, J.R. Miell, M. Modo, S.C. Williams, W.P. Cawthorn, G. Medina-Gomez, A. Vidal-Puig et al. IGF-binding protein-2 protects against the development of obesity and insulin resistance. Diabetes 56, 285–294 (2007)CrossRefPubMedPubMedCentral S.B. Wheatcroft, M.T. Kearney, A.M. Shah, V.E. Ezzat, J.R. Miell, M. Modo, S.C. Williams, W.P. Cawthorn, G. Medina-Gomez, A. Vidal-Puig et al. IGF-binding protein-2 protects against the development of obesity and insulin resistance. Diabetes 56, 285–294 (2007)CrossRefPubMedPubMedCentral
10.
go back to reference J. Frystyk, C. Skjærbæk, E. Vestbo, S. Fisker, H. Ørskov, Circulating levels of free insulin-like growth factors in obese subjects: the impact of type 2 diabetes. Diabetes Metab. Res. Rev. 15, 314–322 (1999)CrossRefPubMed J. Frystyk, C. Skjærbæk, E. Vestbo, S. Fisker, H. Ørskov, Circulating levels of free insulin-like growth factors in obese subjects: the impact of type 2 diabetes. Diabetes Metab. Res. Rev. 15, 314–322 (1999)CrossRefPubMed
11.
go back to reference R.M. Martin, J.M.P. Holly, G.D. Smith, D. Gunnel, Associations of adiposity from childhood into adulthood with Insulin Resistance and the Insulin-like growth factor system: 65-year follow-up of the Boyd Orr Cohort. J. Clin. Endocrinol. Metab. 9, 3287–3295 (2006)CrossRef R.M. Martin, J.M.P. Holly, G.D. Smith, D. Gunnel, Associations of adiposity from childhood into adulthood with Insulin Resistance and the Insulin-like growth factor system: 65-year follow-up of the Boyd Orr Cohort. J. Clin. Endocrinol. Metab. 9, 3287–3295 (2006)CrossRef
12.
go back to reference W. Ruan, M. Lai, Insulin-like growth factor binding protein: a possible marker for the metabolic syndrome? Acta Diabetol. 1, 5–14 (2010)CrossRef W. Ruan, M. Lai, Insulin-like growth factor binding protein: a possible marker for the metabolic syndrome? Acta Diabetol. 1, 5–14 (2010)CrossRef
13.
go back to reference S. Carter, Z. Li, I. Lemieux, N. Alméras, A. Tremblay, J. Bergeron, P. Poirier, Y. Deshaies, J.P. Després, F. Picard, Circulating IGFBP-2 levels are incrementally linked to correlates of the metabolic syndrome and independently associated with VLDL triglycerides. Atherosclerosis. 2, 645–651 (2014)CrossRef S. Carter, Z. Li, I. Lemieux, N. Alméras, A. Tremblay, J. Bergeron, P. Poirier, Y. Deshaies, J.P. Després, F. Picard, Circulating IGFBP-2 levels are incrementally linked to correlates of the metabolic syndrome and independently associated with VLDL triglycerides. Atherosclerosis. 2, 645–651 (2014)CrossRef
14.
go back to reference S.A. Halim, M.L. Neely, K.S. Pieper, S.H. Shah, W.E. Kraus, E.R. Hauser, R.M. Califf, C.B. Granger, L.K. Newby, Simultaneous consideration of multiple candidate protein biomarkers for long-term risk for cardiovascular events. Circ. Cardiovasc. Genet. 1, 168–177 (2015)CrossRef S.A. Halim, M.L. Neely, K.S. Pieper, S.H. Shah, W.E. Kraus, E.R. Hauser, R.M. Califf, C.B. Granger, L.K. Newby, Simultaneous consideration of multiple candidate protein biomarkers for long-term risk for cardiovascular events. Circ. Cardiovasc. Genet. 1, 168–177 (2015)CrossRef
15.
go back to reference E. Asilmaz, P. Cohen, M. Miyazaki, P. Dobrzyn, K. Ueki, G. Fayzikhodjaeva, A.A. Soukas, C.R. Kahn, J.M. Ntambi, N.D. Socci et al. Site and mechanism of leptin action in a rodent form of congenital lipodystrophy. J. Clin. Invest. 3, 414–424 (2004)CrossRef E. Asilmaz, P. Cohen, M. Miyazaki, P. Dobrzyn, K. Ueki, G. Fayzikhodjaeva, A.A. Soukas, C.R. Kahn, J.M. Ntambi, N.D. Socci et al. Site and mechanism of leptin action in a rodent form of congenital lipodystrophy. J. Clin. Invest. 3, 414–424 (2004)CrossRef
16.
go back to reference K. Hedbacker, K. Birsoy, R.W. Wysocki, E. Asilmaz, R.S. Ahima, I.S. Farooqi, J.M. Friedman, Antidiabetic effects of IGFBP2, a Leptin-Regulated Gene. Cell. Metab. 11, 11–22 (2010)CrossRefPubMed K. Hedbacker, K. Birsoy, R.W. Wysocki, E. Asilmaz, R.S. Ahima, I.S. Farooqi, J.M. Friedman, Antidiabetic effects of IGFBP2, a Leptin-Regulated Gene. Cell. Metab. 11, 11–22 (2010)CrossRefPubMed
17.
go back to reference U.H. Neumann, S. Chen, Y.Y. Tam, R.K. Baker, S.D. Covey, P.R. Cullis, T.J. Kieffer, IGFBP2 is neither sufficient nor necessary for the physiological actions of leptin on glucose homeostasis in male ob/ob mice. Endocrinology 3, 716–725 (2014)CrossRef U.H. Neumann, S. Chen, Y.Y. Tam, R.K. Baker, S.D. Covey, P.R. Cullis, T.J. Kieffer, IGFBP2 is neither sufficient nor necessary for the physiological actions of leptin on glucose homeostasis in male ob/ob mice. Endocrinology 3, 716–725 (2014)CrossRef
18.
go back to reference S. Manning, A. Pucci, N.C. Carter, M. Elkalaawy, G. Querci, S. Magno, A. Tamberi, N. Finer, A.G. Fiennes, M. Hashemi et al. Early postoperative weight loss predicts maximal weight loss after sleeve gastrectomy and Roux-en-Y gastric bypass. Surg. Endosc. 6, 1484–1491 (2015)CrossRef S. Manning, A. Pucci, N.C. Carter, M. Elkalaawy, G. Querci, S. Magno, A. Tamberi, N. Finer, A.G. Fiennes, M. Hashemi et al. Early postoperative weight loss predicts maximal weight loss after sleeve gastrectomy and Roux-en-Y gastric bypass. Surg. Endosc. 6, 1484–1491 (2015)CrossRef
19.
go back to reference G. Ceccarini, A.M. Ciccarone, F. Santini, S. Del Prato, Integrating medical and surgical therapies to optimize the outcomes of type 2 diabetes. Surg. Obes. Relat. Dis. 6, 1186–1191 (2016)CrossRef G. Ceccarini, A.M. Ciccarone, F. Santini, S. Del Prato, Integrating medical and surgical therapies to optimize the outcomes of type 2 diabetes. Surg. Obes. Relat. Dis. 6, 1186–1191 (2016)CrossRef
20.
go back to reference V. Lonut, R.N. Bergman, Mechanisms responsible for excess weight loss after bariatric surgery. J. Diabetes. Sci. Technol. 5, 1263–1282 (2011)CrossRef V. Lonut, R.N. Bergman, Mechanisms responsible for excess weight loss after bariatric surgery. J. Diabetes. Sci. Technol. 5, 1263–1282 (2011)CrossRef
21.
go back to reference D.E. Cummings, J. Overduin, K.E. Foster-Shubert, Gastric Bypass for obesity: mechanisms of weight loss and diabetes resolution. J. Clin. Endocrinol. Metab. 6, 2608–2615 (2004)CrossRef D.E. Cummings, J. Overduin, K.E. Foster-Shubert, Gastric Bypass for obesity: mechanisms of weight loss and diabetes resolution. J. Clin. Endocrinol. Metab. 6, 2608–2615 (2004)CrossRef
22.
go back to reference C.N. Ochner, C. Gibson, M. Shanik, V. Goel, A. Geliebter, Changes in neurohormonal gut peptides following bariatric surgery. Int. J. Obes. 2, 153–166 (2011)CrossRef C.N. Ochner, C. Gibson, M. Shanik, V. Goel, A. Geliebter, Changes in neurohormonal gut peptides following bariatric surgery. Int. J. Obes. 2, 153–166 (2011)CrossRef
23.
go back to reference M. Bose, S. Machineni, B. Oliván, J. Teixeira, J.J. McGinty, B. Bawa, N. Koshy, A. Colarusso, B. Laferrère. Superior appetite hormone profile after equivalent weight loss by gastric bypass compared to gastric banding. Obesity 6, 1085–1091 (2010) M. Bose, S. Machineni, B. Oliván, J. Teixeira, J.J. McGinty, B. Bawa, N. Koshy, A. Colarusso, B. Laferrère. Superior appetite hormone profile after equivalent weight loss by gastric bypass compared to gastric banding. Obesity 6, 1085–1091 (2010)
24.
go back to reference J.M. Friedman, Leptin and the regulation of body weight. Keio J. Med. 1, 1–9 (2011)CrossRef J.M. Friedman, Leptin and the regulation of body weight. Keio J. Med. 1, 1–9 (2011)CrossRef
25.
go back to reference G. Ceccarini, M. Maffei, P. Vitti, F. Santini, Fuel homeostasis and locomotor behavior: role of leptin and melanocortin pathways. J. Endocrinol. Invest. 2, 125–131 (2015)CrossRef G. Ceccarini, M. Maffei, P. Vitti, F. Santini, Fuel homeostasis and locomotor behavior: role of leptin and melanocortin pathways. J. Endocrinol. Invest. 2, 125–131 (2015)CrossRef
26.
go back to reference Z. Hao, M.B. Mumphrey, C.D. Morrison, H. Münzberg, J. Ye, H.R. Berthoud, Does gastric bypass surgery change body weight set point? Int. J. Obes. Suppl 1, S37–S43 (2016)CrossRef Z. Hao, M.B. Mumphrey, C.D. Morrison, H. Münzberg, J. Ye, H.R. Berthoud, Does gastric bypass surgery change body weight set point? Int. J. Obes. Suppl 1, S37–S43 (2016)CrossRef
28.
go back to reference M.B. Ranke, R. Schweizer, M.W. Elmlinger, K. Weber, G. Binder, C.P. Schwarze, H.A. Wollmann, Significance of basal IGF-I, IGFBP-3 and IGFBP-2 measurements in the diagnostics of short stature in children. Horm. Res. 2, 60–68 (2000) M.B. Ranke, R. Schweizer, M.W. Elmlinger, K. Weber, G. Binder, C.P. Schwarze, H.A. Wollmann, Significance of basal IGF-I, IGFBP-3 and IGFBP-2 measurements in the diagnostics of short stature in children. Horm. Res. 2, 60–68 (2000)
29.
go back to reference D.E. Arterburn, M.K. Olsen, V.A. Smith, E.H. Livingston, L. Van Scoyoc, W.S. Yancy Jr, G. Eid, H. Weidenbacher, M.L. Maciejewski, Association between bariatric surgery and long-term survival. JAMA. 313, 62–70 (2015)CrossRef D.E. Arterburn, M.K. Olsen, V.A. Smith, E.H. Livingston, L. Van Scoyoc, W.S. Yancy Jr, G. Eid, H. Weidenbacher, M.L. Maciejewski, Association between bariatric surgery and long-term survival. JAMA. 313, 62–70 (2015)CrossRef
30.
go back to reference L. Sjöström, Bariatric surgery and reduction in morbidity and mortality: experiences from the SOS study. Int. J. Obes. Suppl 7, S93–S97 (2008)CrossRef L. Sjöström, Bariatric surgery and reduction in morbidity and mortality: experiences from the SOS study. Int. J. Obes. Suppl 7, S93–S97 (2008)CrossRef
31.
go back to reference C.D. Morrison, Leptin resistance and the response to positive energy balance. Physiol. Behav. 5, 660–663 (2008)CrossRef C.D. Morrison, Leptin resistance and the response to positive energy balance. Physiol. Behav. 5, 660–663 (2008)CrossRef
32.
go back to reference H. Cui, M. López, K. Rahmouni, The cellular and molecular bases of leptin and ghrelin resistance in obesity. Nat Rev Endocrinol. 6, 338–351 (2017)CrossRef H. Cui, M. López, K. Rahmouni, The cellular and molecular bases of leptin and ghrelin resistance in obesity. Nat Rev Endocrinol. 6, 338–351 (2017)CrossRef
33.
go back to reference Z. Li, J. Martin, P. Poirier, S.M. Caron-Cantin, F.S. Hould, S. Marceau, P. Marceau, F. Picard, Upregulation of Plasma Insulin-like growth factor binding protein 2 levels after biliopancreatic diversion in humans. Obesity. 7, 1469–1473 (2012)CrossRef Z. Li, J. Martin, P. Poirier, S.M. Caron-Cantin, F.S. Hould, S. Marceau, P. Marceau, F. Picard, Upregulation of Plasma Insulin-like growth factor binding protein 2 levels after biliopancreatic diversion in humans. Obesity. 7, 1469–1473 (2012)CrossRef
34.
go back to reference J.B. Dixon, N.E. Straznicky, E.A. Lambert, M.P. Schlaich, G.W. Lambert, Surgical approaches to the treatment of obesity. Nat Rev Gastroenterol Hepatol. 8, 429–437 (2011)CrossRefPubMed J.B. Dixon, N.E. Straznicky, E.A. Lambert, M.P. Schlaich, G.W. Lambert, Surgical approaches to the treatment of obesity. Nat Rev Gastroenterol Hepatol. 8, 429–437 (2011)CrossRefPubMed
35.
go back to reference M. Ahrens, O. Ammerpohl, W. von Schönfels, J. Kolarova, S. Bens, T. Itzel, A. Teufel, A. Herrmann, M. Brosch, H. Hinrichsen et al. DNA methylation analysis in nonalcoholic fatty liver disease suggests distinct disease-specific and remodeling signatures after bariatric surgery. Cell. Metab. 2, 296–302 (2013)CrossRef M. Ahrens, O. Ammerpohl, W. von Schönfels, J. Kolarova, S. Bens, T. Itzel, A. Teufel, A. Herrmann, M. Brosch, H. Hinrichsen et al. DNA methylation analysis in nonalcoholic fatty liver disease suggests distinct disease-specific and remodeling signatures after bariatric surgery. Cell. Metab. 2, 296–302 (2013)CrossRef
36.
go back to reference W.J. Smith, L.E. Underwood, D.R. Clemmons, Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J. Clin. Endocrinol. Metab. 2, 443–449 (1995) W.J. Smith, L.E. Underwood, D.R. Clemmons, Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J. Clin. Endocrinol. Metab. 2, 443–449 (1995)
37.
go back to reference V. Touskova, P. Trachta, P. Kavalkova, J. Drapalova, D. Haluzikova, M. Mraz, Z. Lacinova, J. Marek, M. Haluzik, Serum concentrations and tissue expression of components of insulin-like growth factor-axis in females with type 2 diabetes mellitus and obesity: the influence of very-low-calorie diet. Mol. Cell. Endocrinol. 1–2, 172–178 (2012) V. Touskova, P. Trachta, P. Kavalkova, J. Drapalova, D. Haluzikova, M. Mraz, Z. Lacinova, J. Marek, M. Haluzik, Serum concentrations and tissue expression of components of insulin-like growth factor-axis in females with type 2 diabetes mellitus and obesity: the influence of very-low-calorie diet. Mol. Cell. Endocrinol. 12, 172–178 (2012)
38.
go back to reference Z. Hao, H. Münzberg, K. Rezai-Zadeh, M. Keenan, D. Coulon, H. Lu, H.R. Berthoud, J. Ye, Leptin deficient ob/ob mice and diet-induced obese mice responded differently to Roux-en-Y bypass surgery. Int. J. Obes. 5, 798–805 (2015)CrossRef Z. Hao, H. Münzberg, K. Rezai-Zadeh, M. Keenan, D. Coulon, H. Lu, H.R. Berthoud, J. Ye, Leptin deficient ob/ob mice and diet-induced obese mice responded differently to Roux-en-Y bypass surgery. Int. J. Obes. 5, 798–805 (2015)CrossRef
40.
go back to reference J.D. Roth, B.L. Roland, R.L. Cole, J.L. Trevaskis, C. Weyer, J.E. Koda, C.M. Anderson, D.G. Parkes, A.D. Baron, Leptin responsiveness restored by amylin agonism indiet-induced obesity: Evidence from nonclinical and clinical studies. Proc. Natl. Acad. Sci. USA 20, 7257–7262 (2008)CrossRef J.D. Roth, B.L. Roland, R.L. Cole, J.L. Trevaskis, C. Weyer, J.E. Koda, C.M. Anderson, D.G. Parkes, A.D. Baron, Leptin responsiveness restored by amylin agonism indiet-induced obesity: Evidence from nonclinical and clinical studies. Proc. Natl. Acad. Sci. USA 20, 7257–7262 (2008)CrossRef
41.
go back to reference J.L. Trevaskis, T. Coffey, R. Cole, C. Lei, C. Wittmer, B. Walsh, C. Weyer, J. Koda, A.D. Baron, D.G. Parkes et al. Amylin-mediated restoration of leptin responsiveness indiet-induced obesity: magnitude and mechanisms. Endocrinology 11, 5679–5687 (2008)CrossRef J.L. Trevaskis, T. Coffey, R. Cole, C. Lei, C. Wittmer, B. Walsh, C. Weyer, J. Koda, A.D. Baron, D.G. Parkes et al. Amylin-mediated restoration of leptin responsiveness indiet-induced obesity: magnitude and mechanisms. Endocrinology 11, 5679–5687 (2008)CrossRef
42.
go back to reference J. Korner, R. Conroy, G. Febres, D.J. McMahon, I. Conwell, W. Karmally, L.J. Aronne, Randomized double-blind placebo-controlled study of leptin administration after gastric bypass. Obesity. 5, 951–956 (2013)CrossRef J. Korner, R. Conroy, G. Febres, D.J. McMahon, I. Conwell, W. Karmally, L.J. Aronne, Randomized double-blind placebo-controlled study of leptin administration after gastric bypass. Obesity. 5, 951–956 (2013)CrossRef
43.
go back to reference K. Miyako, L.J. Cobb, M. Francis, A. Huang, B. Peng, J.E. Pintar, H. Ariga, P. Cohen, Is a nuclear binding partner of IGFBP-2 and modulates its growth-promoting actions. Mol. Endocrinol. 2, 169–175 (2009)CrossRef K. Miyako, L.J. Cobb, M. Francis, A. Huang, B. Peng, J.E. Pintar, H. Ariga, P. Cohen, Is a nuclear binding partner of IGFBP-2 and modulates its growth-promoting actions. Mol. Endocrinol. 2, 169–175 (2009)CrossRef
44.
go back to reference W.J. Azar, S. Zivkovic, G.A. Werther, V.C. Russo, IGFBP-2 nuclear translocation is mediated by a functional NLS sequence and is essential for its pro-tumorigenic actions in cancer cells. Oncogene 5, 578–588 (2014)CrossRef W.J. Azar, S. Zivkovic, G.A. Werther, V.C. Russo, IGFBP-2 nuclear translocation is mediated by a functional NLS sequence and is essential for its pro-tumorigenic actions in cancer cells. Oncogene 5, 578–588 (2014)CrossRef
45.
go back to reference K.W. Frommer, K. Reichenmiller, B.S. Schutt, A. Hoeflich, M.B. Ranke, G. Dodt, M.W. Elmlinger, IGF-indipendent effects of IGFBP-2 on the human breast cancer cell line Hs578T. J. Mol. Endocrinol. 1, 13–23 (2006)CrossRef K.W. Frommer, K. Reichenmiller, B.S. Schutt, A. Hoeflich, M.B. Ranke, G. Dodt, M.W. Elmlinger, IGF-indipendent effects of IGFBP-2 on the human breast cancer cell line Hs578T. J. Mol. Endocrinol. 1, 13–23 (2006)CrossRef
46.
go back to reference S.B. Wheatcroft, M.T. Kearney, IGF-dependent and IGF-independent actions of IGF-binding protein-1 e –2: implications for metabolic homeostasis. Trends. Endocrinol. Metab. 4, 153–162 (2009)CrossRef S.B. Wheatcroft, M.T. Kearney, IGF-dependent and IGF-independent actions of IGF-binding protein-1 e –2: implications for metabolic homeostasis. Trends. Endocrinol. Metab. 4, 153–162 (2009)CrossRef
Metadata
Title
Serum IGF-binding protein 2 (IGFBP-2) concentrations change early after gastric bypass bariatric surgery revealing a possible marker of leptin sensitivity in obese subjects
Authors
Giovanni Ceccarini
Caterina Pelosini
Federica Ferrari
Silvia Magno
Jacopo Vitti
Guido Salvetti
Carlo Moretto
Antonio Marioni
Piero Buccianti
Paolo Piaggi
Margherita Maffei
Ferruccio Santini
Publication date
01-07-2019
Publisher
Springer US
Published in
Endocrine / Issue 1/2019
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-019-01915-y

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