Low circulating levels of IGF-1 in healthy adults are associated with reduced β-cell function, increased intramyocellular lipid, and enhanced fat utilization during fasting

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 6, 2014, Pages 2198-2207

  Thankamony, Ajay ^a   Capalbo, Donatella ^a   Marcovecchio, M Loredana ^a   Sleigh, Alison ^b   Jørgensen, Sine Wanda ^e   Hill, Nathan R ^f   Mooslehner, Katrin ^a   Yeo, Giles S H ^b   Bluck, Les ^c   Juul, Anders ^g   Vaag, Allan ^e   Dunger, David B ^a,d  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MRC HUMAN NUTRITION RESEARCH   (United Kingdom)

^d MRC Human Nutrition Research of Growth and Reproduction Biomedical Research Centre ^*  (United Kingdom)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ADIPONECTIN; C PEPTIDE; CARNITINE PALMITOYLTRANSFERASE I; GLUCOSE TRANSPORTER 1; GLYCEROL; INSULIN; MALONYL COENZYME A DECARBOXYLASE; SOMATOMEDIN C;

ADULT; AREA UNDER THE CURVE; ARTICLE; BODY COMPOSITION; CALORIMETRY; CELL FUNCTION; CONTROLLED STUDY; CPT1A GENE; DIET RESTRICTION; DOWN REGULATION; FATTY ACID METABOLISM; GENE; GENE EXPRESSION REGULATION; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; GLUT1 GENE; HUMAN; INSULIN RELEASE; INSULIN SENSITIVITY; LIPID METABOLISM; MALE; MUSCLE BIOPSY; MYLCD GENE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; UPREGULATION;

ADOLESCENT; ADULT; FASTING; GLUCOSE; HEALTH; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INSULIN-SECRETING CELLS; LIPID METABOLISM; LIPIDS; MALE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; YOUNG ADULT;

EID: 84902324728     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-4542     Document Type: Article

References (41)

1. LeRoith D, Yakar S. Mechanisms of disease: metabolic effects of growth hormone and insulin-like growth factor 1. Nat Clin Pract Endocrinol Metab. 2007;3:302-310.
2. Kulkarni RN, Holzenberger M, Shih DQ, et al.-Cell-specific deletion of the Igf1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter-cell mass. Nat Genet. 2002;31:111-115.
3. Dupuis J, Langenberg C, Prokopenko I, et al. New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat Genet. 2010;42:105-116.
4. Friedrich N, Thuesen B, Jørgensen T, et al. The association between IGF-I and insulin resistance: a general population study in Danish adults. Diabetes Care. 2012;35:768-773.
5. Sesti G, Sciacqua A, Cardellini M, et al. Plasma concentration of IGF-I is independently associated with insulin sensitivity in subjects with different degrees of glucose tolerance. Diabetes Care. 2005; 28:120-125.
6. SandhuMS,HealdAH,Gibson JM, et al. Circulating concentrations of insulin-like growth factor-I and development of glucose intolerance: a prospective observational study. Lancet. 2002;359:1740-1745.
7. Rajpathak SN He M Sun Q et al Insulin-like growth factor axis and risk of type 2 diabetes in women Diabetes. 2012 61 2248-2254.
8. Shishko PI, Kovalev PA, Goncharov VG, Zajarny IU. Comparison of peripheral and portal (via the umbilical vein) routes of insulin infusion in IDDM patients. Diabetes. 1992;41:1042-1049.
9. Mø ller N, Jørgensen JO. Effects of growth hormone on glucose, lipid, and protein metabolism in human subjects. Endocr Rev. 2009; 30:152-177.
10. Dendrou CA, Plagnol V, Fung E, et al. Cell-specific prote in phenotypes for the autoimmune locus IL2RA using a genotype-selectable human bioresource. Nat Genet. 2009;41:1011-1015.
11. Jensen RB, Thankamony A, O 'Connell SM, et al. Baseline IGF-I levels d etermine insulin secretion and insulin sensitivity during the first year on growth hormone therapy in children born small for gestational age. Results from a North European Multicentre Study (NESGAS). Horm Res Paediatr. 2013;80:38-46 .
12. Salgin B, Marcovecchio ML, Humphreys SM, et al. Effects of prolonged fasting and sustained lipolysis on insulin secretion and insulin sensitivity in normal subjects. Am J Physiol Endocrinol Metab. 2009; 296:E454-E461.
13. Elia M, Livesey G. Energy expenditure and fuel selection in biological systems: the theory and practice of calculations based on indirect calorimetry and tracer methods. World Rev Nutr Die t. 1992;70: 68-131.
14. Semple RK, Sleigh A, Murgatroyd PR, et al. Postreceptor insulin resistance contributes to human dyslipidemia and hepatic steatosis. J Clin Invest. 2009;119:315-322.
15. Sleigh A, Raymond-Barker P, Thackray K, et al. Mitochondrial dysfunction in patients with primary congenital insulin resistance. J Clin Invest. 2011;121:2457-2461.
16. Salgin B, Marcovecchio ML, Williams RM, et al. Effects of growth hormone and free fatty acids on insulin sensitivity in patients with type 1 diabetes. J Clin Endocrinol Metab. 2009;94:3297-3305.
17. Jovanovic Z, Tung YC,LamBY, O 'Rahilly S, Yeo GS. Identification of the global transcriptomic response of the hypothalamic arcuate nucleus to fasting and leptin. J Neuroendocrinol. 2010;22:915-9 25.
18. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care. 2004;27:1487-1495.
19. Fontana L, Weiss EP, Villareal DT, Klein S, Holloszy JO. Long-term effects of calorie or protein restriction on serum IGF-1 and IGFBP-3 concentration in humans. Aging Cell. 2008;7:681-687.
20. Harrela M, Koistinen H, Kaprio J, et al. Genetic and environmenta l components of interindividual variation in circulating levels of IGF-I, IGF-II, IGFBP-1, and IGFBP-3. J Clin Invest. 1996;98:2612-2615.
21. Verkauskiene R, Jaquet D, Deghmoun S, Chevenne D, Czer nichow P, Levy-Marchal C. Smallness for gestational age is associated with persistent change in insulin-like growth factor I (IGF-I) and the ratio of IGF-I/IGF-binding protein-3 in adulthood. J Clin Endocrinol Metab. 2005;90: 5672-5676.
22. OngKK,Petry CJ,EmmettPM,et al. Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth, and plasma insulin-like growth factor-I levels. Diabetologia. 2004;47: 106 4-1070.
23. Chirieac DV, Chirieac LR, Corsetti JP, Cianci J, Sparks CE, Sparks JD. Glucose-stimulated insulin secretion suppresses hepatic triglyceride-rich lipoprotein and apoB production. Am J Physiol Endocrinol Metab. 2000;279:E1003-E1011.
24. Ciaraldi TP, Mudaliar S, Barzin A, et al. Skeletal muscle GLUT1 transporter protein expression and basal leg glucose uptake are reduced in type 2 diabetes. J Clin Endocrinol Metab. 2005;90:352-358.
25. Dí az M, Vraskou Y, Gutiérrez J, Planas JV. Expression of rainbow trout glucose transporters GLUT1 and GLUT4 during in vitro muscle cell differentiati on and regulation by insulin and IGF-1. Am J Physiol Regul Integr Comp Physiol. 2009;296:R794-R800.
26. Parekh N, Roberts CB, Vadiveloo M, Puvananayagam T, Albu JB, Lu-Yao GL. Lifestyle, anthr opometric, and obesity-related physiologic determinants of insulin-like growth factor-1 in the Third National Health and Nutrition Examination Survey (1988-1994).Ann Epidemiol. 2010;20:182-193.
27. Succ urro E, Andreozzi F, Marini MA, et al. Low plasma insulin-like growth factor-1 levels are associated with reduced insulin sensitivity and increased insulin secretion in nondiabetic subjects. Nutr Metab Cardiovasc Dis. 2009;1 9:713-719.
28. Ib ánez L López-Bermejo A Dí az M Marcos MV Casano P de Zegher F Abdominal fat partitioning and high-molecular-weight adiponectin in short children born small for gestational age. J Clin Endocrinol Metab.2009 94 1049-1052.
29. Semple RK, Cochran EK, Soos MA, et al. Plasma adiponectin as a marker of insulin receptor dysfunction: clinical utility in severe insulin resistance. Diabetes Care. 2008;31:977-979.
30. Gosby AK, Maloney CA, Caterson ID. Elevated insulin sensitivity in low-protein offspring rats is prevented by a high-fa t diet and is associated with visceral fat. Obesity. 2010;18:1593-1600.
31. List EO, Sackmann-Sala L, Berryman DE, Funk K, et al. Endocrine parameters and phenotypes of the growth hormone re ceptor gene disrupted (GHR-/-) mouse. Endocr Rev. 2011;32:356-386.
32. Watt MJ, Hoy AJ. Lipid metabolism in skeletal muscle: generation of adaptive and maladaptive intracellular signals for cellular fun ction. Am J Physiol Endocrinol Metab. 2012;302:E1315-E1328.
33. Ziouzenkova O, Orasanu G, Sharlach M, et al. Retinaldehyde represses adipogenesis and diet-induced obesity. Nat Med. 2007;13: 695-702.
34. Cameron-Smith D, Burke LM, Angus DJ, et al. A short-term, highfat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am J Clin Nutr. 2003;77:313-318.
35. Jensen MD. Regional glycerol and free fatty acid metabolism before and after meal ingestion. Am J Physiol. 1999;276:E863-E869.
36. Coen PM, Goodpaster BH. R ole of intramyocelluar lipids in human health. Trends Endocrinol Metab. 2012;23:391-398.
37. Stannard SR, Johnson NA. Insulin resistance and elevated triglyceride in muscle: more important for survival than "thrifty" genes? J Physiol. 2004;554:595-607.
38. Nø rrelund H. The metabolic role of growth hormone in humans with particular reference to fasting. Growth Horm IGF Res. 2005; 15:95-122.
39. Hofman PL, Cutfield WS, Robinson EM, et al. Insulin resistance in short children with intrauterine growth retardation. J Clin Endocrinol Metab. 1997;82:402-406.
40. Bazaes RA, Salazar TE, Pittaluga E, et al. Glucose and lipid metabolism in small for gestational age infants at 48 hours of age. Pediatrics. 2003;111:804-809.
41. Salgin B, Marcovecchio ML, Humphreys SM, et al. Effects of prolonged fasting and sustained lipolysis on insulin secretion and insulin sensitivity in normal subjects. Am J Physiol Endocrinol Metab. 2009;296:E454-E461.