The metabolic effects of growth hormone in adipose tissue

Endocrine

Volumn 44, Issue 2, 2013, Pages 293-302

  Chaves, Valéria Ernestânia ^a   Júnior, Fernando Mesquita ^b   Bertolini, Gisele Lopes ^b  

^a FEDERAL UNIVERSITY OF SÃO JOÃO DEL REI   (Brazil)

^b FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

Author keywords

Adipose tissue; Growth hormone; Metabolism of lipids; Obesity; Signal transduction pathways

Indexed keywords

GROWTH HORMONE; GROWTH HORMONE RECEPTOR; GROWTH HORMONE RELEASING FACTOR; HORMONE SENSITIVE LIPASE; JANUS KINASE 2; LONG CHAIN FATTY ACID COENZYME A LIGASE; RECOMBINANT GROWTH HORMONE; SOMATOMEDIN C; STAT5 PROTEIN; TRIACYLGLYCEROL;

ABDOMINAL FAT; ABDOMINAL OBESITY; ADIPOGENESIS; ADIPOSE TISSUE; BODY FAT DISTRIBUTION; BODY MASS; GROWTH HORMONE DEFICIENCY; GROWTH HORMONE RELEASE; HUMAN; HYPOPITUITARISM; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; METABOLIC SYNDROME X; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; WEIGHT REDUCTION;

ADIPOGENESIS; ADIPOSE TISSUE; ADULT; ANIMALS; GROWTH HORMONE; HUMAN GROWTH HORMONE; HUMANS; HYPOPITUITARISM; LIPID METABOLISM;

EID: 84885630101     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-013-9904-3     Document Type: Review

References (117)

1. R.G. Rosenfeld, Growth hormone deficiency in children, in Endocrinology, ed. by L.J. Degroot, J.L. Jameson (W.B. Saunders, Philadelphia, 2001), pp. 503-519
2. J.O.L. Jorgensen, L. Moller, M. Krag, N. Billestrup, J.S. Christiansen, Effects of growth hormone on glucose and fat metabolism in human subjects. Endocrinol. Metab. Clin. N. Am. 36, 75-87 (2007)
3. N. Moller, K.C. Copeland, K.S. Nair, Growth hormone effects on protein metabolism. Endocrinol. Metab. Clin. N. Am. 36, 89-100 (2007)
4. N. Moller, J.O.L. Jorgensen, Effects of growth hormone on glucose, lipid, and protein metabolism in human subjects. Endocr. Rev. 30, 152-177 (2009)
5. Y. Wang, S.K. Fried, R.N. Petersen, P.A. Schoknecht, Somatotropin regulates adipose tissue metabolism in neonatal swine. J. Nutr. 129, 139-145 (1999)
6. D.M. Harris, F.R. Dunshea, D.E. Bauman, R.D. Boyd, S.Y. Wang, P.A. Johnson, S.D. Clarke, Effect of in vivo somatotropin treatment of growing pigs on adipose tissue lipogenesis. J. Anim. Sci. 71, 3293-3300 (1993)
7. M. Wabitsch, E. Heinze, Body fat in GH-deficient children and the effect of treatment. Horm. Res. 40, 5-9 (1993)
8. J.D. Veldhuis, A. Iranmanesh, K.K. Ho, M.J. Waters, M.L. Johnson, G. Lizarralde, Dual defects in pulsatile growth hormone secretion and clearance subserve the hyposomatotropism of obesity in man. J. Clin. Endocrinol. Metab. 72, 51-59 (1991)
9. S.A. Beshyah, A. Henderson, R. Niththyanathan, P. Sharp, W. Richmond, D.G. Johnston, Metabolic abnormalities in growth hormone-deficient adults. II: Carbohydrate tolerance and lipid metabolism. Endocrinol. Metab. 1, 173-180 (1994)
10. M.L. Vance, N. Mauras, Growth hormone therapy in adults and children. N. Eng. J. Med. 341, 1206-1214 (1999)
11. A.L. Utz, A. Yamamoto, L. Hemphill, K.K. Miller, Growth hormone deficiency by growth hormone releasing hormone-arginine testing criteria predicts increased cardiovascular risk markers in normal young overweight and obese women. J. Clin. Endocrinol. Metab. 93, 2507-2514 (2008)
12. M. Gola, S. Bonadonna, M. Doga, A. Giustina, Clinical review: Growth hormone and cardiovascular risk factors. J. Clin. Endocrinol. Metab. 90, 1864-1870 (2005)
13. M. Gola, S. Bonadonna, M. Doga, G. Mazziotti, A. Giustina, Cardiovascular risk in aging and obesity: is there a role for GH. J. Endocrinol. Invest. 28, 759-767 (2005)
14. L. Li, W. Ren, J. Li, J. Liu, L. Wang, X. Zheng, D. Liu, S. Li, R. Souvenir, J. Tang, Increase in serum pregnancy-associated plasma protein-A is correlated with increase in cardiovascular risk factors in adult patients with growth hormone deficiency. Endocrine 42, 375-381 (2012)
15. M. Doga, S. Bonadonna, M. Gola, S.B. Solerte, G. Amato, C. Carella, A. Giustina, Current guidelines for adult GH replacement. Rev. Endocr. Metab. Disord. 6, 63-70 (2005)
16. M. Gola, A. Giustina, Growth hormone deficiency and cardiovascular risk: do we need additional markers? Endocrine 42, 240-242 (2012)
17. M.H. Rasmussen, Obesity, growth hormone and weight loss. Mol. Cell. Endocrinol. 316, 147-153 (2010)
18. A. Iranmanesh, G. Lizarralde, J.D. Veldhuis, Age and relative adiposity are specific negative determinants of the frequency and amplitude of growth hormone (GH) secretory bursts and the half-life of endogenous GH in healthy men. J. Clin. Endocrinol. Metab. 73, 1081-1088 (1991)
19. E. Kamycheva, V. Berg, R. Jorde, Insulin-like growth factor I, growth hormone, and insulin sensitivity: the effects of a one-year cholecalciferol supplementation in middle-aged overweight and obese subjects. Endocrine. (2012) [Epub ahead of print]
20. M.E. Molitch, D.R. Clemmons, S. Malozowski, G.R. Merriam, M.L. Vance, Evaluation and treatment of adult growth hormone deficiency: An endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab. 96, 1587-1609 (2011)
21. U.J. Lewis, R.N. Singh, G.H. Tutwiler, M.B. Sigel, E.F. VanderLaan, W.P. VanderLaan, Human growth hormone: a complex of proteins. Recent Prog. Horm. Res. 36, 477-508 (1980)
22. S.S. Abdel-Meguid, H.S. Shieh, W.W. Smith, H.E. Dayringer, B.N. Violand, L.A. Bentle, Three-dimensional structure of a genetically engineered variant of porcine growth hormone. Proc. Natl. Acad. Sci. U.S.A. 84, 6434-6437 (1987)
23. A.C. Gore, J.L. Roberts, Neuroendocrine systems, in Fundamental Neuroscience, ed. by L.R. Squire, F.E. Bloom, S.K. McConnell (Elsevier Science, San Diego, 2003), pp. 1031-1065
24. M. Barinaga, G. Yamonoto, C. Rivier, W. Vale, R. Evans, M.G. Rosenfeld, Transcriptional regulation of growth hormone gene expression by growth hormone-releasing factor. Nature 306, 84-85 (1983)
25. R.W. Holl, M.O. Thorner, D.A. Leong, Intracellular calcium concentration and growth hormone secretion in individual somatotropes: effects of growth hormone-releasing factor and somatostatin. Endocrinology 122, 2927-2932 (1988)
26. A. Giustina, J.D. Velhuis, Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr. Rev. 19, 717-797 (1998)
27. E.O. Reiter, R.G. Rosenfeld, Normal and aberrant growth, in Williams Textbook of Endocrinology, ed. by P.R. Larsen, H.M. Kronenberg, S. Melmed, K.S. Polonski (Elsevier Science, San Diego, 2003), pp. 1009-1014
28. P. Barnett, Somatostatin and somatostatin receptor physiology. Endocrine 20, 255-264 (2003)
29. M.L. Hartman, A.C.S. Faria, M.L. Vance, M.T. Johnson, M.O. Thorner, J.D. Veldhuis, Temporal structure of in vivo growth hormone secretory events in humans. Am. J. Physiol. 260, E101-E110 (1991)
30. N. Goldenberg, A. Barkan, Factors regulating growth hormone secretion in humans. Endocrinol. Metab. Clin. North Am. 36, 37-55 (2007)
31. M. Berelowitz, M. Szabo, L.A. Frohman, L.A. Frohman, S. Firestone, L. Chu, R.L. Hintz, Somatomedin-C mediates growth hormone negative feedback by effects on both the hypothalamus and pituitary. Science 212, 1279-1281 (1981)
32. C.Y. Bowers, F. Momany, G.A. Reynolds, A. Hong, On the in vitro and in vivo activity of a new synthetic hexapeptide that acts on the pituitary to specifically release growth hormone. Endocrinology 114, 1537-1545 (1984)
33. S. Yamashita, S. Melmed, Insulin-like growth factor I action on rat anterior pituitary cells: suppression of growth hormone secretion and messenger ribonucleic acid levels. Endocrinology 118, 176-182 (1986)
34. R.G. Rosenfeld, G. Ceda, C.W. Cutler, L.A. Dollar, A.R. Hoffman, Insulin and insulin-like growth factor (somatomedin) receptors on cloned rat pituitary tumor cells. Endocrinology 117, 2008-2016 (1985)
35. G.P. Ceda, R.G. Davis, R.G. Rosenfeld, A.R. Hoffman, The growth hormone (GH) releasing hormone (GHRH)/GH/somatomedin axis: evidence for rapid inhibition of GHRH-elicited GH release by insulin-like growth factors I and II. Endocrinology 120, 1658-1662 (1987)
36. M.A. Vaccarello, F.B. Diamond Jr, J. Guevara-Aguirre, A.L. Rosenbloom, P.J. Fielder, S. Gargosky, P. Cohen, K. Wilson, R.G. Rosenfeld, Hormonal and metabolic effects and pharmacokinetics of recombinant insulin-like growth factor I in growth hormone receptor deficiency (GHRD)/Laron syndrome. J. Clin. Endocrinol. Metab. 77, 273-280 (1993)
37. J. Bellone, G. Aimaretti, E. Bartolotta, L. Benso, B.P. Imbimbo, V. Lenhaerts, R. Deghenghi, F. Camanni, E. Ghigo, Growth hormone-releasing activity of hexarelin, a new synthetic hexapeptide, before and during puberty. Clin. Endocrinol. Metab. 80, 1090-1094 (1995)
38. M. Korbonits, A.B. Grossman, Growth hormone-releasing peptide and its analogues. Trends Endocrinol. Metab. 6, 43-49 (1995)
39. R. Birnbacher, S. Riedl, H. Frisch, Long-term treatment in children with hypopituitarism: Pubertal development and final height. Horm. Res. 49, 80-85 (1998)
40. K. Takaya, H. Ariyasu, N. Kanamoto, H. Iwakura, A. Yoshimoto, M. Harada, K. Mori, Y. Komatsu, T. Usui, A. Shimatsu, Y. Ogawa, K. Hosoda, T. Akamizu, M. Kojima, K. Kangawa, K. Nakao, Ghrelin strongly stimulates growth hormone (GH) release in humans. J. Clin. Endocrinol. Metab. 85, 4908-4911 (2000)
41. A.M.J. Lengyel, From growth hormone-releasing peptides to ghrelin: discovery of new modulators of GH secretion. Arq. Bras. Endocrinol. Metab. 50, 17-24 (2006)
42. D.G. Gardner, R.A. Nissenson, Mechanisms of hormone action, in Greenspan's Basic & Clinical Endocrinology, ed. by D.G. Gardner, D. Shoback (McGraw-Hill Medical, New York, 2007), pp. 36-57
43. R.J. Brown, J.J. Adams, R.A. Pelekanos, Y. Wan, W.J. McKinstry, K. Palethorpe, R.M. Seeber, T.A. Monks, K.A. Eidne, M.W. Parker, M.J. Waters, Model for growth hormone receptor activation based on subunit rotation within a receptor dimer. Nat. Struct. Mol. Biol. 12, 814-821 (2005)
44. N.J. Lanning, C. Carter-Su, Recent advances in growth hormone signaling. Rev. Endocr. Metab. Disord. 7, 225-235 (2006)
45. L.S. Argetsinger, G.S. Campbell, X. Yang, B.A. Witthuhn, O. Silvennoinen, J.N. Ihle, C. Carter-Su, Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 74, 237-244 (1993)
46. L.H. Hansen, X. Wang, J.J. Kopchick, P. Bouchelouche, J.H. Nielsen, E.D. Galsgaard, N. Billestrup, Identification of tyrosine residues in the intracellular domain of the growth hormone receptor required for transcriptional signaling and Stat5 activation. J. Biol. Chem. 271, 12669-12673 (1996)
47. N. Carpino, R. Kobayashi, H. Zang, Y. Takahashi, S.T. Jou, J. Feng, H. Nakajima, J.N. Ihle, Identification, cDNA cloning, and targeted deletion of p70, a novel, ubiquitously expressed SH3 domaincontaining protein. Mol. Cell. Biol. 22, 7491-7500 (2002)
48. T. Zhu, L. Ling, P.E. Lobie, Identification of a JAK2-independent pathway regulating growth hormone (GH)-stimulated p44/42 mitogen activated protein kinase activity. GH activation of Ral and phospholipase D is Src-dependent. J. Biol. Chem. 277, 45592-45603 (2002)
49. N. Asada, Y. Takahashi, M. Wada, N. Naito, H. Uchida, M. Ikeda, M. Honjo, GH induced lipolysis stimulation in 3T3-L1 adipocytes stably expressing hGHR: analysis on signaling pathway and activity of 20 K hGH. Mol. Cell. Endocrinol. 162, 121-129 (2000)
50. J.N. Fain, J.H. Ihle, S.W. Bahouth, Stimulation of lipolysis but not of leptin release by growth hormone is abolished in adipose tissue from Stat5a and b knockout mice. Biochem. Biophys. Res. Commun. 263, 201-205 (1999)
51. J.O.L. Jorgensen, N. Jessen, S.B. Pedersen, E. Vestergaard, L. Gormsen, S.A. Lund, N. Billestrup, Growth hormone receptor signaling in skeletal muscle and adipose tissue in human subjects following exposure to an intravenous GH bolus. Am. J. Physiol. Endocrinol. Metab. 291, E899-E905 (2006)
52. L. Moller, L. Dalman, H. Norrelund, N. Billestrup, J. Frystyk, N. Moller, J.O.L. Jorgensen, Impact of fasting on growth hormone signaling and action in muscle and fat. J. Clin. Endocrinol. Metab. 94, 965-972 (2009)
53. A.C.P. Thirone, C.R.O. Carvalho, M.J.A. Saad, Growth hormone stimulates the tyrosine kinase activity of JAK2 and induces tyrosine phosphorylation of insulin receptor substrates and Shc in rat tissues. Endocrinology 140, 55-62 (1999)
54. N. Yang, Y. Huang, J. Jiang, S.J. Frank, Caveolar and lipid raft localization of the growth hormone receptor and its signaling elements: impact on growth hormone signaling. J. Biol. Chem. 279, 20898-20905 (2004)
55. C.M. Szego, A. White, The influence of purified growth hormone on fasting metabolism. J. Clin. Endocrinol. Metab. 8, 594 (1948)
56. K. Chihara, K. Fujieda, A. Shimatsu, T. Miki, K. Tachibana, Dose-dependent changes in body composition during growth hormone (GH) treatment in Japanese patients with adult GH deficiency: a randomized, placebo-controlled trial. Growth Horm. IGF Res. 20, 205-211 (2010)
57. P.V. Carroll, W.M. Drake, K.T. Maher, K. Metcalfe, N.J. Shaw, D.B. Dunger, T.D. Cheetham, C. Camacho-Hubner, M.O. Savage, J.P. Monson, Comparison of continuation or cessation of growth hormone (GH) therapy on body composition and metabolic status in adolescents with severe GH deficiency at completion of linear growth. J. Clin. Endocrinol. Metab. 89, 3890-3895 (2004)
58. P.J. Collipp, J. Thomas, V. Curti, R.K. Sharma, V.T. Maddaiah, S.E. Cohn, Body composition changes in children receiving human growth hormone. Metabolism. 22, 589-595 (1973)
59. D.E. Berryman, E.O. List, D.T. Kohn, K.T. Coschigano, R.J. Seeley, J.J. Kopchick, Effect of growth hormone on susceptibility to diet-induced obesity. Endocrinology 147, 2801-2808 (2006)
60. A. Vijayakumar, R. Novosyadlyy, Y. Wu, S. Yakar, D. LeRoith, Biological effects of growth hormone on carbohydrate and lipid metabolism. Growth Horm. IGF Res. 20, 1-7 (2010)
61. J.T. Zhao, M.J. Cowley, P. Lee, V. Birzniece, W. Kaplan, K.K.Y. Ho, Identification of novel GH-regulated pathway of lipid metabolism in adipose tissue: a gene expression study in hypopituitary men. J. Clin. Endocrinol. Metab. 96, 1-9 (2011)
62. S. Yang, H. Mulder, C. Holm, S. Eden, Effects of growth hormone on the function of beta-adrenoceptor subtypes in rat adipocytes. Obes. Res. 12, 330-339 (2004)
63. R. Doris, R.G. Vernon, M.D. Houslay, E. Kilgour, Growth hormone decreases the response to anti-lipolytic agonists and decreases the levels of Gi2 in rat adipocytes. Biochem. J. 297, 41-45 (1994)
64. R.A. Doris, E. Kilgour, M.D. Houslay, R.G. Vernon, Regulation of the GTP-binding protein-based antilipolytic system of sheep adipocytes by growth hormone. J. Endocrinol. 158, 295-303 (1998)
65. V.E. Chaves, D. Frasson, N.H. Kawashita, Several agents and pathways regulate lipolysis in adipocytes. Biochimie 93, 1631-1640 (2011)
66. V.E. Chaves, D. Frasson, M.E. Martins-Santos, R.P. Boschini, M.A. Garófalo, W.T. Festuccia, I.C. Kettelhut, R.H. Migliorini, Glyceroneogenesis is reduced and glucose uptake is increased in adipose tissue from cafeteria diet-fed rats independently of tissue sympathetic innervation. J. Nutr. 136, 2475-2480 (2006)
67. K.A. Magri, M. Adamo, D. LeRoith, T.D. Etherton, The inhibition of insulin action and glucose metabolism by porcine growth hormone in porcine adipocytes is not the result of any decrease in insulin binding or insulin receptor kinase activity. Biochem. J. 266, 107-113 (1990)
68. E. Kilgour, S.A. Baldwin, D.J. Flint, Divergent regulation of rat adipocyte GLUT1 and GLUT4 glucose transporters by GH. J. Endocrinol. 145, 27-33 (1995)
69. C.Y. Liu, A.L. Grant, K.H. Kim, S.E. Mills, Porcine somatotropin decreases acetyl-coA carboxylase gene expression in porcine adipose tissue. Domest. Anim. Endocrinol. 11, 125-132 (1994)
70. I. Louveau, F. Gondret, GH and insulin affect fatty acid synthase activity in isolated porcine adipocytes in culture without any modifications of sterol regulatory element binding protein-1 expression. J. Endocrinol. 181, 271-280 (2004)
71. S.S. Donkin, P.Y. Chiu, D. Yin, I. Louveau, B. Swencki, J. Vockroth, C.M. Evock-Clover, J.L. Peters, T.D. Etherton, Porcine somatotropin differentially down-regulates expression of the GLUT4 and fatty acid synthase genes in pig adipose tissue. J. Nutr. 126, 2568-2577 (1996)
72. A.M. Mildner, S.D. Clarke, Porcine fatty acid synthase: cloning of a complementary DNA, tissue distribution of its mRNA and suppression of expression by somatotropin and dietary protein. J. Nutr. 121, 900-907 (1991)
73. C.F. Semenkovich, Regulation of fatty acid synthase. Prog. Lipid Res. 36, 43-53 (1997)
74. D. Yin, S.D. Clarke, J.L. Peters, T.D. Etherton, Somatotropin-dependent decrease in fatty acid synthase mRNA abundance in 3T3-F442A adipocytes is the result of a decrease in both gene transcription and mRNA stability. Biochem. J. 331, 815-820 (1998)
75. R.M. Catalioto, G. Ailhaud, R. Negrel, Diacylglycerol production induced by growth hormone in Ob1771 preadipocytes arises from phosphatidylcholine breakdown. Biochem. Biophys. Res. Commun. 173, 840-848 (1990)
76. T. Johansen, B. Richelsen, H.S. Hansen, N. Din, K. Malmlof, Growth hormone mediated breakdown of body fat: effects of GH on lipases in adipose tissue and skeletal muscle of old rats fed different diets. Horm. Metab. Res. 35, 243-250 (2003)
77. Y. Khalfallah, G. Sassolas, F. Borson-Chazot, N. Vega, H. Vidal, Expression of insulin target genes in skeletal muscle and adipose tissue in adult patients with growth hormone deficiency: effect of one year recombinant human growth hormone therapy. J. Endocrinol. 171, 285-292 (2001)
78. B. Richelsen, S.B. Pedersen, K. Kristensen, J.D. Borglum, H. Norrelund, J.S. Christiansen, J.O.L. Jorgensen, Regulation of lipoprotein lipase and hormone-sensitive lipase activity and gene expression in adipose and muscle tissue by growth hormone treatment during weight loss in obese patients. Metabolism. 49, 906-911 (2000)
79. J. Oscarsson, M. Ottosson, S. Eden, Effects of growth hormone on lipoprotein lipase and hepatic lipase. J. Endocrinol. Invest. 22, 2-9 (1999)
80. T. Nixon, H. Green, Contribution of growth hormone to the adipogenic activity of serum. Endocrinology 114, 527-532 (1984)
81. M. Kawai, N. Namba, S. Mushiake, Y. Etani, R. Nishimura, M. Makishima, K. Ozono, Growth hormone stimulates adipogenesis of 3T3-L1 cells through activation of the STAT5a/5b-PPARgamma pathway. J. Mol. Endocrinol. 38, 19-34 (2007)
82. C. Lu, P.A. Kumar, Y. Fan, M.A. Sperling, R.K. Menon, A novel effect of growth hormone on macrophage modulates macrophage-dependent adipocyte differentiation. Endocrinology 151, 2189-2199 (2010)
83. W.P. Arend, S. D'Angelo, F.G. Joslin, Regulation of interleukin 1 production in human monocytes. I. Effects of gamma-interferon and cycloheximide. Clin. Exp. Immunol. 74, 377-381 (1988)
84. 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)
85. S. Gesta, Y.H. Tseng, C.R. Kahn, Developmental origin of fat: tracking obesity to its source. Cell 131, 242-256 (2007)
86. M.C. Arkan, A.L. Hevener, F.R. Greten, S. Maeda, Z.W. Li, J.M. Long, A. Wynshaw-Boris, G. Poli, J. Olefsky, M. Karin, IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 11, 191-198 (2005)
87. K.M. Rexrode, V.J. Carey, C.H. Hennekens, E.E. Walters, G.A. Colditz, M.J. Stampfer, W.C. Willett, J.E. Manson, Abdominal adiposity and coronary heart disease in women. JAMA 280, 1843-1848 (1998)
88. J. Nedergaard, B. Cannon, The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab. 11, 268-272 (2010)
89. D.W. Haslam, W.P. James, Obesity. Lancet. 366, 1197-1209 (2006)
90. E. Ferrannini, S.M. Haffner, B.D. Mitchell, M.P. Stern, Hyperinsulinemia: the key feature of a cardiovascular and metabolic syndrome. Diabetologia 3, 416-422 (1991)
91. K.K. Miller, B.M.K. Biller, J.G. Lipman, G. Bradwin, N. Rifai, A. Klibanski, Truncal adiposity, relative growth hormone deficiency, and cardiovascular risk. J. Clin. Endocrinol. Metab. 90, 768-774 (2005)
92. J. Argente, N. Caballo, V. Barrios, J. Pozo, M.T. Muñiz, J.A. Chowen, M. Hernández, 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. 82, 2076-2083 (1997)
93. R.M. Luque, R.D. Kineman, Impact of obesity on the growth hormone axis: evidence for a direct inhibitory effect of hyperinsulinemia on pituitary function. Endocrinology 147, 2754-2763 (2006)
94. H. Vakili, Y. Jin, P.A. Cattini, Negative regulation of human growth hormone gene expression by insulin is dependent on hypoxia-inducible factor binding in primary non-tumor pituitary cells. J. Biol. Chem. 287, 33282-33292 (2012)
95. N. Attia, W.V. Tamborlane, R. Heptulla, D. Maggs, A. Grozman, R.S. Sherwin, S. Caprio, The metabolic syndrome and insulin-like growth factor I regulation in adolescent obesity. J. Clin. Endocrinol. Metab. 83, 1467-1471 (1998)
96. E. Ghigo, G. Aimaretti, L. Gianotti, J. Bellone, E. Arvat, F. Camanni, New approach to the diagnosis of growth hormone deficiency in adults. Eur. J. Endocrinol. 134, 352-356 (1996)
97. L.B. Tankó, J.M. Bruun, P. Alexandersen, Y.Z. Bagger, B. Richelsen, C. Christiansen, P.J. Larsen, Novel associations between bioavailable estradiol and adipokines in elderly women with different phenotypes of obesity: implications for atherogenesis. Circulation 110, 2246-2252 (2004)
98. D. Styne, Growth, in Greenspan's Basic & Clinical Endocrinology, ed. by D.G. Gardner, D. Shoback (McGraw-Hill Medical, New York, 2007), pp. 171-206
99. A.S. Bates, W. Van't Hoff, P.J. Jones, R.N. Clayton, The effect of hypopituitarism on life expectancy. J. Clin. Endocrinol. Metab. 81, 1169-1172 (1996)
100. J.D.J. Thomas, J.P. Monson, Adult GH deficiency throughout lifetime. Eur. J. Endocrinol. 161, S97-S106 (2009)
101. D.E. Cummings, G.R. Merriam, Growth hormone therapy in adults. Annu. Rev. Med. 54, 513-533 (2003)
102. F. Salomon, R. Cuneo, R. Hesp, P. Sönksen, The effects of treatment with recombinant human growth hormone on body composition and metabolism in adults with growth hormone deficiency. N. Engl. J. Med. 321, 1221-1225 (1989)
103. A. Binnerts, G.R. Swart, J.H.P. Wilson, N. Hoogerbrugge, H.A. Pols, J.C. Birkenhager, S.W. Lamberts, The effect of growth hormone administration in growth hormone deficient adults on bone, protein, carbohydrate and lipid homeostasis, as well as body composition. Clin. Endocrinol. 37, 79-87 (1992)
104. J.U. Weaver, J.P. Monson, K. Noonan, W.G. John, A. Edwards, K.A. Evans, J. Cunningham, The effect of low dose recombinant human growth hormone replacement on regional fat distribution, insulin sensitivity and cardiovascular risk factors in hypopituitary adults. J. Clin. Endocrinol. Metab. 80, 153-159 (1995)
105. A. Chrisolidou, S. Beshyah, O. Rutherford, T.J. Spinks, J. Mayet, P. Kyd, V. Anyaoku, A. Haida, B. Ariff, M. Murphy, E. Thomas, S. Robinson, R. Foale, D.G. Johnston, Effects of seven years of growth hormone replacement therapy in hypopituitary adults. J. Clin. Endocrinol. Metab. 85, 3762-3769 (2000)
106. M.H. Rasmussen, A. Hvidberg, A. Juul, K.M. Main, A. Gotfredsen, N.E. Skakkebaek, J. Hilsted, N.E. Skakkebae, Massive Weight loss restores 24-hour growth hormone release profiles and serum insulin-like growth factor-I levels in obese subjects. J. Clin. Endocrinol. Metab. 80, 1407-1415 (1995)
107. S. Shadid, M.D. Jensen, Effects of growth hormone administration in human obesity. Obes. Res. 11, 170-175 (2003)
108. S.G. Albert, A.D. Mooradian, Low-dose recombinant human growth hormone as adjuvant therapy to lifestyle modifications in the management of obesity. J. Clin. Endocrinol. Metab. 89, 695-701 (2004)
109. C.W. Ahn, C.S. Kim, J.H. Nam, H.J. Kim, J.S. Nam, J.S. Park, E.S. Kang, B.S. Cha, S.K. Lim, K.R. Kim, H.C. Lee, K.B. Hub, Effects of growth hormone on insulin resistance and atherosclerotic risk factors in obese type 2 diabetic patients with poor glycaemic control. Clin. Endocrinol. 64, 444-449 (2006)
110. C. Franco, J. Brandberg, L. Lönn, B. Andersson, B.A. Bengtsson, G. Johannsson, Growth hormone treatment reduces abdominal visceral fat in postmenopausal women with abdominal obesity: a 12-month placebo-controlled trial. J. Clin. Endocrinol. Metab. 90, 1466-1474 (2005)
111. M. Pasarica, J.J. Zachwieja, L. Dejonge, S. Redman, S.R. Smith, Effect of growth hormone on body composition and visceral adiposity in middle-aged men with visceral obesity. J. Clin. Endocrinol. Metab. 92, 4265-4270 (2007)
112. T. Rosen, B.A. Bengtsson, Premature mortality due to cardiovascular disease in hypopituitarism. Lancet 336, 285-288 (1990)
113. T.A. Abdu, R. Neary, T.A. Elhadd, M. Akber, R.N. Clayton, Coronary risk in growth hormone deficient hypopituitary adults: increased predicted risk is due largely to lipid profile abnormalities. Clin. Endocrinol. 55, 209-216 (2001)
114. A. Besson, S. Salemi, S. Gallati, A. Jenal, R. Horn, P.S. Mullis, P.E. Mullis, Reduced longevity in untreated patients with isolated growth hormone deficiency. J. Clin. Endocrinol. Metab. 88, 3664-3667 (2003)
115. E.M. Erfurth, B. Bulow, J. Eskilsson, L. Hagmar, High incidence of cardiovascular disease and increased prevalence of cardiovascular risk factors in women with hypopituitarism not receiving growth hormone treatment: preliminary results. Growth Horm. IGF Res. 9, A21-A24 (1999)
116. J.U. Weaver, J.P. Monson, K. Noonan, W.G. John, A. Edwards, K.A. Evans, J. Cunningham, The effect of low dose recombinant human growth hormone replacement on regional fat distribution, insulin sensitivity, and cardiovascular risk factors in hypopituitary adults. J. Clin. Endocrinol. Metab. 80, 153-159 (1995)
117. J.O. Jorgensen, N. Vahl, T.B. Hansen, L. Thuesen, C. Hagen, J.S. Christiansen, Growth hormone versus placebo treatment for one year in growth hormone deficient adults: increase in exercise capacity and normalization of body composition. Clin. Endocrinol. 45, 681-688 (1996)