Neuroendocrine alterations in the exercising human: Implications for energy homeostasis

Metabolism: Clinical and Experimental

Volumn 62, Issue 7, 2013, Pages 911-921

  Fuqua, John S ^a   Rogol, Alan D ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cortisol; Energy expenditure; Ghrelin; Hypogonadism; Leptin

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; GHRELIN; GLUCAGON; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GONADORELIN; GROWTH HORMONE RELEASING FACTOR; HYDROCORTISONE; INCRETIN; KISSPEPTIN; LEPTIN; PEPTIDE YY; SOMATOMEDIN;

ADENOHYPOPHYSIS; ADVERSE OUTCOME; ALPHA ADRENERGIC RECEPTOR BLOCKING; ANDROGEN RELEASE; ANOREXIA NERVOSA; APPETITE; ARCUATE NUCLEUS; BODY FAT; BONE DENSITY; CALORIC INTAKE; CARDIOVASCULAR DISEASE; ENERGY BALANCE; ENERGY EXPENDITURE; ESTROGEN DEFICIENCY; EXERCISE; FEEDBACK SYSTEM; FOOD INTAKE; GENITAL SYSTEM; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GONADOTROPIN SECRETING CELL; HOMEOSTASIS; HORMONE RELEASE; HUMAN; HYDROCORTISONE RELEASE; HYPOGONADISM; HYPOGONADOTROPIC HYPOGONADISM; HYPOPHYSIS; HYPOPHYSIS FUNCTION; HYPOTHALAMIC AMENORRHEA; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; INSULIN RELEASE; INSULIN SENSITIVITY; LEPTIN DEFICIENCY; LIPODYSTROPHY; MENTAL STRESS; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; PRECOCIOUS PUBERTY; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SATIETY; SOLITARY TRACT NUCLEUS;

ANIMALS; APPETITE REGULATION; ENERGY METABOLISM; EXERCISE; GHRELIN; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LEPTIN; NEUROSECRETORY SYSTEMS; SATIETY RESPONSE;

EID: 84879552113     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.01.016     Document Type: Review

References (77)

1. Y. Zhang, R. Proenca, and M. Maffei Positional cloning of the mouse obese gene and its human homologue Nature 372 6505 1994 425 432
2. C.T. Montague, I.S. Farooqi, and J.P. Whitehead Congenital leptin deficiency is associated with severe early-onset obesity in humans Nature 387 6636 1997 903 908
3. A. Strobel, T. Issad, and L. Camoin A leptin missense mutation associated with hypogonadism and morbid obesity Nat Genet 18 3 1998 213 215
4. I.S. Farooqi, S.A. Jebb, and G. Langmack Effects of recombinant leptin therapy in a child with congenital leptin deficiency N Engl J Med 341 12 1999 879 884
5. M. Kojima, H. Hosoda, and Y. Date Ghrelin is a growth-hormone-releasing acylated peptide from stomach Nature 402 6762 1999 656 660
6. Y. Date, M. Kojima, and H. Hosoda Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans Endocrinology 141 11 2000 4255 4261
7. A.M. Wren, L.J. Seal, and M.A. Cohen Ghrelin enhances appetite and increases food intake in humans J Clin Endocrinol Metab 86 12 2001 5992
8. D.E. Cummings, D.S. Weigle, and R.S. Frayo Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery N Engl J Med 346 21 2002 1623 1630
9. M. Tena-Sempere Ghrelin: novel regulator of gonadal function J Endocrinol Invest 28 5 Suppl 2005 26 29
10. C. Broberger, J. Johansen, and C. Johansson The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice Proc Natl Acad Sci USA 95 25 1998 15043 15048
11. J. Kamegai, H. Tamura, and T. Shimizu Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats Diabetes 50 11 2001 2438 2443
12. D. Huszar, C.A. Lynch, and V. Fairchild-Huntress Targeted disruption of the melanocortin-4 receptor results in obesity in mice Cell 88 1 1997 131 141
13. R.D. Cone Anatomy and regulation of the central melanocortin system Nat Neurosci 8 5 2005 571 578
14. C.W. le Roux, R.L. Batterham, and S.J. Aylwin Attenuated peptide YY release in obese subjects is associated with reduced satiety Endocrinology 147 1 2006 3 8
15. M.R. Hayes, L. Bradley, and H.J. Grill Endogenous hindbrain glucagon-like peptide-1 receptor activation contributes to the control of food intake by mediating gastric satiation signaling Endocrinology 150 6 2009 2654 2659
16. M. Granado, C. Garcia-Caceres, and L.M. Frago The positive effects of growth hormone-releasing peptide-6 on weight gain and fat mass accrual depend on the insulin/glucose status Endocrinology 151 5 2010 2008 2018
17. H.R. Berthoud Metabolic and hedonic drives in the neural control of appetite: who is the boss? Curr Opin Neurobiol 21 6 2011 888 896
18. B.K. Anand, and J.R. Brobeck Localization of a "feeding center" in the hypothalamus of the rat Proc Soc Exp Biol Med 77 2 1951 323 324
19. G.A. Bray Historical framework for the development of ideas about obesity G.A. Bray, C. Bouchard, W.P.T. James, Handbook of Obesity 1998 CRC Press Boca Raton, FL 6
20. L. Gautron, and J.K. Elmquist Sixteen years and counting: an update on leptin in energy balance J Clin Invest 121 6 2011 2087 2093
21. S. Kamohara, R. Burcelin, and J.L. Halaas Acute stimulation of glucose metabolism in mice by leptin treatment Nature 389 6649 1997 374 377
22. L. Rossetti, D. Massillon, and N. Barzilai Short term effects of leptin on hepatic gluconeogenesis and in vivo insulin action J Biol Chem 272 44 1997 27758 27763
23. W. Fan, D.M. Dinulescu, and A.A. Butler The central melanocortin system can directly regulate serum insulin levels Endocrinology 141 9 2000 3072 3079
24. C.F. Elias, C. Lee, and J. Kelly Leptin activates hypothalamic CART neurons projecting to the spinal cord Neuron 21 6 1998 1375 1385
25. M.D. Barrachina, V. Martinez, and L. Wang Synergistic interaction between leptin and cholecystokinin to reduce short-term food intake in lean mice Proc Natl Acad Sci USA 94 19 1997 10455 10460
26. T.R. Castaneda, J. Tong, and R. Datta Ghrelin in the regulation of body weight and metabolism Front Neuroendocrinol 31 1 2010 44 60
27. D.L. Williams, D.G. Baskin, and M.W. Schwartz Hindbrain leptin receptor stimulation enhances the anorexic response to cholecystokinin Am J Physiol Regul Integr Comp Physiol 297 5 2009 R1238 R1246
28. J.S. Marino, Y. Xu, and J.W. Hill Central insulin and leptin-mediated autonomic control of glucose homeostasis Trends Endocrinol Metab 22 7 2011 275 285
29. K. Ebihara, T. Kusakabe, and M. Hirata Efficacy and safety of leptin-replacement therapy and possible mechanisms of leptin actions in patients with generalized lipodystrophy J Clin Endocrinol Metab 92 2 2007 532 541
30. K.F. Petersen, E.A. Oral, and S. Dufour Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy J Clin Invest 109 10 2002 1345 1350
31. M.L. Hartman, J.D. Veldhuis, and M.L. Johnson Augmented growth hormone (GH) secretory burst frequency and amplitude mediate enhanced GH secretion during a two-day fast in normal men J Clin Endocrinol Metab 74 4 1992 757 765
32. T.S. Hannon, J. Janosky, and S.A. Arslanian Longitudinal study of physiologic insulin resistance and metabolic changes of puberty Pediatr Res 60 6 2006 759 763
33. D. LeRoith, L. Scavo, and A. Butler What is the role of circulating IGF-I? Trends Endocrinol Metab 12 2 2001 48 52
34. P.M. Martha Jr., K.M. Gorman, and R.M. Blizzard Endogenous growth hormone secretion and clearance rates in normal boys, as determined by deconvolution analysis: relationship to age, pubertal status, and body mass J Clin Endocrinol Metab 74 2 1992 336 344
35. B.S. Keenan, G.E. Richards, and S.W. Ponder Androgen-stimulated pubertal growth: the effects of testosterone and dihydrotestosterone on growth hormone and insulin-like growth factor-I in the treatment of short stature and delayed puberty J Clin Endocrinol Metab 76 4 1993 996 1001
36. D.L. Metzger, and J.R. Kerrigan Estrogen receptor blockade with tamoxifen diminishes growth hormone secretion in boys: evidence for a stimulatory role of endogenous estrogens during male adolescence J Clin Endocrinol Metab 79 2 1994 513 518
37. R. Nogueiras, S. Tovar, and S.E. Mitchell Regulation of growth hormone secretagogue receptor gene expression in the arcuate nuclei of the rat by leptin and ghrelin Diabetes 53 10 2004 2552 2558
38. J.L. Chan, C.J. Williams, and P. Raciti Leptin does not mediate short-term fasting-induced changes in growth hormone pulsatility but increases IGF-I in leptin deficiency states J Clin Endocrinol Metab 93 7 2008 2819 2827
39. M.M. Grumbach A window of opportunity: the diagnosis of gonadotropin deficiency in the male infant J Clin Endocrinol Metab 90 5 2005 3122 3127
40. C.A. Quigley Editorial: The postnatal gonadotropin and sex steroid surge-insights from the androgen insensitivity syndrome J Clin Endocrinol Metab 87 1 2002 24 28
41. R.M. Sharpe, H.M. Fraser, and M.F. Brougham Role of the neonatal period of pituitary-testicular activity in germ cell proliferation and differentiation in the primate testis Hum Reprod 18 10 2003 2110 2117
42. H.M. Dungan, D.K. Clifton, and R.A. Steiner Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion Endocrinology 147 3 2006 1154 1158
43. S.B. Seminara, S. Messager, and E.E. Chatzidaki The GPR54 gene as a regulator of puberty N Engl J Med 349 17 2003 1614 1627
44. M.G. Teles, S.D. Bianco, and V.N. Brito A GPR54-activating mutation in a patient with central precocious puberty N Engl J Med 358 7 2008 709 715
45. J. Roa, V.M. Navarro, and M. Tena-Sempere Kisspeptins in reproductive biology: consensus knowledge and recent developments Biol Reprod 85 4 2011 650 660
46. J.M. Castellano, A.H. Bentsen, and J.D. Mikkelsen isspeptins: bridging energy homeostasis and reproduction Brain Res 1364 2010 129 138
47. C.S. Mantzoros, J.S. Flier, and A.D. Rogol A longitudinal assessment of hormonal and physical alterations during normal puberty in boys V. Rising leptin levels may signal the onset of puberty J Clin Endocrinol Metab 82 4 1997 1066 1070
48. R.V. Garcia-Mayor, M.A. Andrade, and M. Rios Serum leptin levels in normal children: relationship to age, gender, body mass index, pituitary-gonadal hormones, and pubertal stage J Clin Endocrinol Metab 82 9 1997 2849 2855
49. J.N. Roemmich, P.A. Clark, and S.S. Berr Gender differences in leptin levels during puberty are related to the subcutaneous fat depot and sex steroids Am J Physiol 275 3 Pt 1 1998 E543 E551
50. M.B. Horlick, M. Rosenbaum, and M. Nicolson Effect of puberty on the relationship between circulating leptin and body composition J Clin Endocrinol Metab 85 7 2000 2509 2518
51. B.R. King, R.C. Nicholson, and R. Smith Placental corticotrophin- releasing hormone, local effects and fetomaternal endocrinology Stress 4 4 2001 219 233
52. G.P. Chrousos Stress and disorders of the stress system Nat Rev Endocrinol 5 7 2009 374 381
53. D.S. Goldstein, and I.J. Kopin Adrenomedullary, adrenocortical, and sympathoneural responses to stressors: a meta-analysis Endocr Regul 42 4 2008 111 119
54. H. Suga, T. Kadoshima, and M. Minaguchi Self-formation of functional adenohypophysis in three-dimensional culture Nature 480 7375 2011 57 62
55. L. Budry, C. Lafont, and T. El Yandouzi Related pituitary cell lineages develop into interdigitated 3D cell networks Proc Natl Acad Sci USA 108 30 2011 12515 12520
56. A.B. Loucks, M. Verdun, and E.M. Heath Low energy availability, not stress of exercise, alters LH pulsatility in exercising women J Appl Physiol 84 1 1998 37 46
57. N.I. Williams, A.L. Caston-Balderrama, and D.L. Helmreich Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea Endocrinology 142 6 2001 2381 2389
58. N.I. Williams, D.L. Helmreich, and D.B. Parfitt Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training J Clin Endocrinol Metab 86 11 2001 5184 5193
59. A.B. Loucks, and J.R. Thuma Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women J Clin Endocrinol Metab 88 1 2003 297 311
60. K. Pacak, and M. Palkovits Stressor specificity of central neuroendocrine responses: implications for stress-related disorders Endocr Rev 22 4 2001 502 548
61. J.R. Thuma, R. Gilders, and M. Verdun Circadian rhythm of cortisol confounds cortisol responses to exercise: implications for future research J Appl Physiol 78 5 1995 1657 1664
62. K.E. Friedl, R.J. Moore, and R.W. Hoyt Endocrine markers of semistarvation in healthy lean men in a multistressor environment J Appl Physiol 88 5 2000 1820 1830
63. C.K. Welt, J.L. Chan, and J. Bullen Recombinant human leptin in women with hypothalamic amenorrhea N Engl J Med 351 10 2004 987 997
64. S.H. Chou, J.P. Chamberland, and X. Liu Leptin is an effective treatment for hypothalamic amenorrhea Proc Natl Acad Sci USA 108 16 2011 6585 6590
65. E. Sienkiewicz, F. Magkos, and K.N. Aronis Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women Metabolism 60 9 2011 1211 1221
66. C.M. Gordon Leptin and the skeleton-where is the fat? Metabolism 60 9 2011 1203 1206
67. M. Kluge, P. Schussler, and M. Uhr Ghrelin suppresses secretion of luteinizing hormone in humans J Clin Endocrinol Metab 92 8 2007 3202 3205
68. K.E. Ackerman, K. Slusarz, and G. Guereca Higher ghrelin and lower leptin secretion are associated with lower LH secretion in young amenorrheic athletes compared with eumenorrheic athletes and controls Am J Physiol Endocrinol Metab 302 7 2012 E800 E806
69. E. O'Donnell, J.M. Goodman, and P.J. Harvey Clinical review: cardiovascular consequences of ovarian disruption: a focus on functional hypothalamic amenorrhea in physically active women J Clin Endocrinol Metab 96 12 2011 3638 3648
70. G. Karsenty The mutual dependence between bone and gonads J Endocrinol 213 2 2012 107 114
71. G. Karsenty, and M. Ferron The contribution of bone to whole-organism physiology Nature 481 7381 2012 314 320
72. V. Schwetz, T. Pieber, and B. Obermayer-Pietsch The endocrine role of the skeleton: background and clinical evidence Eur J Endocrinol 166 6 2012 959 967
73. N.K. Lee, H. Sowa, and E. Hinoi Endocrine regulation of energy metabolism by the skeleton Cell 130 3 2007 456 469
74. K. Christo, R. Prabhakaran, and B. Lamparello Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects Pediatrics 121 6 2008 1127 1136
75. K.E. Ackerman, T. Nazem, and D. Chapko Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls J Clin Endocrinol Metab 96 10 2011 3123 3133
76. K.E. Ackerman, K.T. Patel, and G. Guereca Cortisol secretory parameters in young exercisers in relation to LH secretion and bone parameters Clin Endocrinol (Oxf) 78 1 2012 114 119
77. M. Russell, J. Stark, and S. Nayak Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls Bone 45 1 2009 104 109