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Research Paper

Associations of GHR, IGF-1 and IGFBP-3 expression in adipose tissue cells with obesity-related alterations in corresponding circulating levels and adipose tissue function in children

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Pages 630-642 | Received 08 Jul 2022, Accepted 14 Nov 2022, Published online: 22 Nov 2022

References

  • Geserick M, Vogel M, Gausche R, et al. Acceleration of BMI in early childhood and risk of sustained obesity. N Engl J Med. 2018 Oct 4;379(14):1303–1312.
  • Kempf E, Vogel M, Vogel T, et al. Dynamic alterations in linear growth and endocrine parameters in children with obesity and height reference values. EClinicalMedicine. 2021 June 23;37:100977.
  • Blum WF, Alherbish A, Alsagheir A, et al. The growth hormone-insulin-like growth factor-I axis in the diagnosis and treatment of growth disorders. Endocr Connect. 2018;7(6):R212–R222.
  • Roelfsema V, Clark RG. The growth hormone and insulin-like growth factor axis: its manipulation for the benefit of growth disorders in renal failure. J Am Soc Nephrol. 2001;12(6):1297.
  • Schilbach K, Bidlingmaier M. Growth hormone binding protein – physiological and analytical aspects. Best Pract Res Clin Endocrinol Metab. 2015 Oct 01;29(5):671–683.
  • Zhang Y, Jiang J, Black RA, et al. Tumor necrosis factor-alpha converting enzyme (TACE) is a growth hormone binding protein (GHBP) sheddase: the metalloprotease TACE/ADAM-17 is critical for (PMA-induced) GH receptor proteolysis and GHBP generation. Endocrinology. 2000 Dec;141(12):4342–4348.
  • Hwa V, Oh Y, Rosenfeld RG. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev. 1999 Dec;20(6):761–787.
  • Ranke MB. Insulin-like growth factor binding-protein-3 (IGFBP–3). Best Pract Res Clin Endocrinol Metab. 2015 Oct 01;29(5):701–711.
  • Haywood NJ, Slater TA, Matthews CJ, et al. The insulin like growth factor and binding protein family: novel therapeutic targets in obesity & diabetes. Mol Metab. 2019 Jan 01;19:86–96.
  • Han VK, Lund PK, Lee DC, et al. Expression of somatomedin/insulin-like growth factor messenger ribonucleic acids in the human fetus: identification, characterization, and tissue distribution. J Clin Endocrinol Metab. 1988 Feb;66(2):422–429.
  • David A, Hwa V, Metherell LA, et al. Evidence for a continuum of genetic, phenotypic, and biochemical abnormalities in children with growth hormone insensitivity. Endocr Rev. 2011 Aug;32(4):472–497.
  • Fusco A, Miele L, D’Uonnolo A, et al. Nonalcoholic fatty liver disease is associated with increased GHBP and reduced GH/IGF-I levels. Clin Endocrinol (Oxf). 2012 Oct;77(4):531–536.
  • Baruch Y, Amit T, Hertz P, et al. Decreased serum growth hormone-binding protein in patients with liver cirrhosis. J Clin Endocrinol Metab. 1991;73(4):777–780.
  • Haluzik M, Yakar S, Gavrilova O, et al. Insulin Resistance in the liver-specific IGF-1 gene-deleted mouse is abrogated by deletion of the acid-labile subunit of the IGF-binding protein-3 complex. Relative roles of growth hormone and IGF-1 in insulin resistance. Diabetes. 2003;52(10):2483–2489.
  • Sjogren K, Liu JL, Blad K, et al. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):7088–7092.
  • Phillips LS, Pao CI, Villafuerte BC. Molecular regulation of insulin-like growth factor-I and its principal binding protein, IGFBP-3. Progress in nucleic acid research and molecular biology. 1998;60:195–265.
  • Wei Y, Rhani Z, Goodyer CG. Characterization of growth hormone receptor messenger ribonucleic acid variants in human adipocytes. J Clin Endocrinol Metab. 2006 May;91(5):1901–1908.
  • Zou L, Menon RK, Sperling MA. Induction of mRNAs for the growth hormone receptor gene during mouse 3T3-L1 preadipocyte differentiation. Metabolism. 1997 Jan;46(1):114–118.
  • Chang HR, Kim HJ, Xu X, et al. Macrophage and adipocyte IGF1 maintain adipose tissue homeostasis during metabolic stresses. Obesity. 2016 Jan;24(1):172–183. (Silver Spring,Md).
  • Møller S, Fisker S, Becker U, et al. A comparison of circulating and regional growth hormone-binding protein in cirrhosis. Metabolism. 2001 November 01;50(11):1340–1345.
  • Yakar S, Liu JL, Stannard B, et al. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7324–7329.
  • Hajer GR, van Haeften TW, Visseren FLJ. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J. 2008;29(24):2959–2971.
  • Kopchick JJ, Berryman DE, Puri V, et al. The effects of growth hormone on adipose tissue: old observations, new mechanisms. Nat Rev Endocrinol. 2020 Mar;16(3):135–146.
  • Scavo LM, Karas M, Murray M, et al. Insulin-like growth factor-I stimulates both cell growth and lipogenesis during differentiation of human mesenchymal stem cells into adipocytes. J Clin Endocrinol Metab. 2004 Jul;89(7):3543–3553.
  • Holly J, Sabin M, Perks C, et al. Adipogenesis and IGF-1. Metab Syndr Relat Disord. 2006;4(1):43–50. Spring.
  • Landgraf K, Friebe D, Ullrich T, et al. Chemerin as a mediator between obesity and vascular inflammation in children. J Clin Endocrinol Metab. 2012 Apr;97(4):E556–64.
  • Johansen MJ, Gade J, Stender S, et al. The effect of overweight and obesity on liver biochemical markers in children and adolescents. J Clin Endocrinol Metab. 2020;105(2):430–442.
  • Landgraf K, Rockstroh D, Wagner IV, et al. Evidence of early alterations in adipose tissue biology and function and its association with obesity-related inflammation and insulin resistance in Children [10.2337/db14-0744]. Diabetes. 2015;64(4):1249–1261.
  • Hadizadeh F, Faghihimani E, Adibi P. Nonalcoholic fatty liver disease: diagnostic biomarkers. World J Gastrointest Pathophysiol. 2017 May 15;8(2):11–26.
  • Ballerini MG, Ropelato MG, Domene HM, et al. Differential impact of simple childhood obesity on the components of the growth hormone-insulin-like growth factor (IGF)-IGF binding proteins axis. J Pediatr Endocrinol Metab. 2004 May;17(5):749–757.
  • Kratzsch J, Dehmel B, Pulzer F, et al. Increased serum GHBP levels in obese pubertal children and adolescents: relationship to body composition, leptin and indicators of metabolic disturbances. Int J Obes Relat Metab Disord. 1997 Dec;21(12):1130–1136.
  • Seminara S, Filpo A, La Cauza F, et al. Growth hormone binding protein activity in obese children. J Endocrinol Invest. 1998 Jul-Aug;21(7):441–444.
  • Argente J, Caballo N, Barrios V, et al. Multiple endocrine abnormalities of the growth hormone and insulin-like growth factor axis in prepubertal children with exogenous obesity: effect of short- and long-term weight reduction. J Clin Endocrinol Metab. 1997 Jul;82(7):2076–2083.
  • Gunnell D, Oliver SE, Donovan JL, et al. Do height-related variations in insulin-like growth factors underlie the associations of stature with adult chronic disease? J Clin Endocrinol Metab. 2004 Jan;89(1):213–218.
  • Hörenz C, Vogel M, Wirkner K, et al. BMI and contraceptives affect new Age-, Sex-, and Puberty-adjusted IGF-I and IGFBP-3 reference ranges across life span. J Clin Endocrinol Metab. 2022 Jun 16;107(7):e2991–e3002.
  • Ong K, Kratzsch J, Kiess W, et al. Circulating IGF-I levels in childhood are related to both current body composition and early postnatal growth rate. J Clin Endocrinol Metab. 2002;87(3):1041–1044.
  • Wabitsch M, Heinze E, Debatin KM, et al. IGF-I- and IGFBP-3-expression in cultured human preadipocytes and adipocytes. Hormone Metab Res. 2000 Nov-Dec;32(11–12):555–559.
  • Fisker S, Hansen B, Fuglsang J, et al. Gene expression of the GH receptor in subcutaneous and intraabdominal fat in healthy females: relationship to GH-binding protein. Eur J Endocrinol/Eur Fed Endocr Soc. 2004 Jun;150(6):773–777.
  • Ross RJ, Esposito N, Shen XY, et al. A short isoform of the human growth hormone receptor functions as a dominant negative inhibitor of the full-length receptor and generates large amounts of binding protein. Mol Endocrinol. 1997 Mar;11(3):265–273. Baltimore, Md.
  • Hesse D, Trost J, Schäfer N, et al. Effect of adipocyte-derived IGF-I on adipose tissue mass and glucose metabolism in the berlin fat mouse. Growth Factors. 2018 Apr;36(1–2):78–88. (Chur, Switzerland).
  • List EO, Berryman DE, Buchman M, et al. Adipocyte-specific GH receptor-Null (AdGHRKO) mice have enhanced insulin sensitivity with reduced liver triglycerides. Endocrinology. 2019 Jan 1;160(1):68–80.
  • List EO, Berryman DE, Funk K, et al. The role of GH in adipose tissue: lessons from adipose-specific GH receptor gene-disrupted mice. Mol Endocrinol. 2013 Mar;27(3):524–535. (Baltimore, Md).
  • Touskova V, Trachta P, Kavalkova P, et al. 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. 2012 Sep 25;361(1):172–178.
  • Glad CAM, Svensson PA, Nystrom FH, et al. Expression of GHR and downstream signaling genes in human adipose tissue-relation to obesity and weight change. J Clin Endocrinol Metab. 2019 May 1;104(5):1459–1470.
  • Campbell KL, Foster-Schubert KE, Makar KW, et al. Gene expression changes in adipose tissue with diet- and/or exercise-induced weight loss. Cancer Prev Res. 2013;6(3):217–231.
  • Blüher S, Kratzsch J, Kiess W. Insulin-like growth factor I, growth hormone and insulin in white adipose tissue. Best Pract Res Clin Endocrinol Metab. 2005 Dec 01;19(4):577–587.
  • Høyer KL, Høgild ML, List EO, et al. The acute effects of growth hormone in adipose tissue is associated with suppression of antilipolytic signals. Physiol Rep. 2020;8(3):e14373.
  • Carrel AL, Allen DB. Effects of growth hormone on adipose tissue. J Pediatr Endocrinol Metab. 2000 Sep;13(Suppl 2):1003–1009.
  • Boucher J, Softic S, El Ouaamari A, et al. Differential roles of insulin and IGF-1 receptors in adipose tissue development and function. Diabetes. 2016;65(8):2201–2213.
  • Boucher J, Tseng Y-H, Kahn CR. Insulin and insulin-like growth factor-1 receptors act as ligand-specific amplitude modulators of a common pathway regulating gene transcription. J Biol Chem. 2010;285(22):17235–17245.
  • Baxter RC, Twigg SM. Actions of IGF binding proteins and related proteins in adipose tissue. Trends Endocrinol Metab. 2009 Dec;20(10):499–505.
  • Chan SSY, Schedlich LJ, Twigg SM, et al. Inhibition of adipocyte differentiation by insulin-like growth factor-binding protein-3. Am J Physiol Endocrinol Metab. 2009 Apr 01;296(4):e654–e663.
  • Lee H, Kim SR, Oh Y, et al. Targeting insulin-like growth factor-I and insulin-like growth factor-binding protein-3 signaling pathways. A novel therapeutic approach for asthma. Am J Respir Cell Mol Biol. 2014 Apr;50(4):667–677.
  • Eliakim A, Nemet D. Exercise training, physical fitness and the growth hormone-insulin-like growth factor-1 axis and cytokine balance. Med Sport Sci. 2010;55:128–140.
  • Rasmussen MH, Juul A, Kjems LL, et al. Effects of short-term caloric restriction on circulating free IGF-I, acid-labile subunit, IGF-binding proteins (IGFBPs)-1-4, and IGFBPs-1-3 protease activity in obese subjects. Eur J Endocrinol/Eur Fed Endocr Soc. 2006 Oct;155(4):575–581.
  • Landgraf K, Klöting N, Gericke M, et al. The obesity-susceptibility gene TMEM18 promotes adipogenesis through activation of PPARG. Cell Rep. 2020;33(3):108295.
  • Kromeyer-Hauschild K, Wabitsch M, Kunze D, et al. Percentiles of body mass index in children and adolescents evaluated from different regional German studies. Monatsschr Kinderh. 2001 Aug;149(8):807–818.
  • Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291–303.
  • Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23.
  • Raschpichler MC, Sorge I, Hirsch W, et al. Evaluating childhood obesity: magnetic resonance-based quanti-fication of abdominal adipose tissue and liver fat in children. RoFo: Fortschritte Auf Dem Gebiete der Rontgenstrahlen Und der Nuklearmedizin. 2012 Apr;184(4):324–332.
  • Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985 July 01;28(7):412–419.
  • Bernhard F, Landgraf K, Klöting N, et al. Functional relevance of genes implicated by obesity genome-wide association study signals for human adipocyte biology. Diabetologia. 2013 Feb;56(2):311–322.