Body weight impact on puberty: Effects of high-calorie diet on puberty onset in female rhesus monkeys

Endocrinology

Volumn 153, Issue 4, 2012, Pages 1696-1705

  Terasawa, Ei ^a,b   Kurian, Joseph R ^a   Keen, Kim L ^a   Shiel, Nicholas A ^a   Colman, Ricki J ^a   Capuano, Saverio V ^a  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE; LEPTIN; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY GROWTH; BODY MASS; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; FEEDING; FEEDING BEHAVIOR; FEMALE; JUVENILE ANIMAL; MENARCHE; METABOLIC DISORDER; MONITORING; NONHUMAN; PRECOCIOUS PUBERTY; PREVALENCE; PRIORITY JOURNAL; PUBERTY; RHESUS MONKEY;

AGING; ANIMALS; BODY MASS INDEX; BODY WEIGHT; ENERGY INTAKE; FEMALE; INSULIN-LIKE GROWTH FACTOR I; LEPTIN; MACACA MULATTA; MENARCHE; MODELS, ANIMAL; OVULATION; SEXUAL MATURATION; TIME FACTORS;

EID: 84859415932     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1970     Document Type: Article

References (72)

1. Styne DM, Grumbach MM 2011 Puberty: ontogeny, neuroendocrinology, physiology, and disorders. In: Melmed S, Polonsky KS, Larsen PR, Kronenberg HM, eds. Williams textbook of endocrinology. 12th ed. Chap 25. Philadelphia: Saunders Elsevier
2. Wyshak G, Frisch RE 1982 Evidence for a secular trend in age of menarche. N Engl J Med 306:1033-1035 (Pubitemid 12155374)
3. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP 2003 The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 24:668-693 (Pubitemid 37330586)
4. Frisch RE, Revelle R 1971 Height and weight at menarche and a hypothesis of menarche. Arch Dis Child 46:695-701
5. Biro FM, McMahon RP, Striegel-Moore R, Crawford PB, Obarzanek E, Morrison JA, Barton BA, Falkner F 2001 Impact of timing of pubertal maturation on growth in black and white female adolescents: the National Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr 138:636-643 (Pubitemid 32417661)
6. Demerath EW, Li J, Sun SS, Chumlea WC, Remsberg KE, Czerwinski SA, Towne B, Siervogel RM 2004 Fifty-year trends in serial body mass index during adolescence in girls: the Fels Longitudinal Study. Am J Clin Nutr 80:441-446 (Pubitemid 41080020)
7. Harris MA, Prior JC, Koehoorn M 2008 Age at menarche in the Canadian population: secular trends and relationship to adulthood BMI. J Adolesc Health 43:548-554
8. Bau AM, Ernert A, Schenk L, Wiegand S, Martus P, Grüters A, Krude H 2009 Is there a further acceleration in the age at onset of menarche? A cross-sectional study in 1840 school children focusing on age and bodyweight at the onset of menarche. Eur J Endocrinol 160:107-113
9. Terasawa E, Noonan JJ, Nass TE, Loose MD 1984 Posterior hypothalamic lesions advance the onset of puberty in the female rhesus monkey. Endocrinology 115:2241-2250 (Pubitemid 15186260)
10. Windsor-Engnell BM, Kasuya E, Mizuno M, Keen KL, Terasawa E 2007 An increase in in vivo release of LHRH and precocious puberty by posterior hypothalamic lesions in female rhesus monkeys (Macaca mulatta). Am J Physiol Endocrinol Metab 292:E1000-E1009 (Pubitemid 46536500)
11. Keen KL, Burich AJ, Mitsushima D, Kasuya E, Terasawa E 1999 Effects of pulsatile infusion of the GABAA receptor blocker bicuculline on the onset of puberty in female rhesus monkeys. Endocrinology 140:5257-5266
12. van Lenthe FJ, Kemper CG, van Mechelen W 1996 Rapid maturation in adolescence results in greater obesity in adulthood: the Amsterdam Growth and Health Study. Am J Clin Nutr 64:18-24
13. Wang Y 2002 Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics 110:903-910 (Pubitemid 35266148)
14. Thompson DR, Obarzanek E, Franko DL, Barton BA, Morrison J, Biro FM, Daniels SR, Striegel-Moore RH 2007 Childhood overweight and cardiovascular disease risk factors: the National Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr 150:18-25 (Pubitemid 44940891)
15. Hamilton AS, Mack TM 2003 Puberty and genetic susceptibility to breast cancer in a case-control study in twins. N Engl J Med 348:2313-2322 (Pubitemid 36638105)
16. Wardle J, Brodersen NH, Cole TJ, Jarvis MJ, Boniface DR 2006 Development of adiposity in adolescence: five year longitudinal study of an ethnically and socioeconomically diverse sample of young people in Britain. BMJ 332:1130-1135
17. Jasik CB, Lustig RH 2008 Adolescent obesity and puberty: the "perfect storm." Ann NY Acad Sci 1135:265-279 (Pubitemid 351862125)
18. Schwartz SM, Wilson ME, Walker ML, Collins DC 1988 Dietary influences on growth and sexual maturation in premenarchial rhesus monkeys. Horm Behav 22:231-251
19. Terasawa E, Nass TE, Yeoman RR, Loose MD, Schultz NJ 1983 Hypo-thalamic control of puberty in the female rhesus macaque. In: Norman RL, ed. Neuroendocrine aspects of reproduction. New York: Academic Press; 149-182
20. Wilson ME, Fisher J, Chikazawa K, Yoda R, Legendre A, Mook D, Gould KG 2003 Leptin administration increases nocturnal concentrations of luteinizing hormone and growth hormone in juvenile female rhesus monkeys. J Clin Endocrinol Metab 88:4874-4883 (Pubitemid 37357538)
21. Blum WF, Englaro P, Hanitsch S, Juul A, Hertel NT, Müller J, Skakkebaek NE, Heiman ML, Birkett M, Attanasio AM, Kiess W, Rascher W 1997 Plasma leptin levels in healthy children and adolescents: dependence on body mass index, body fat mass, gender, pubertal stage, and testosterone. J Clin Endocrinol Metab 82:2904-2910 (Pubitemid 27385646)
22. Quintela M, Señaris R, Heiman ML, Casanueva FF, Dieguez C 1997 Leptin inhibits in vitro hypothalamic somatostatin secretion and somatostatin mRNA levels. Endocrinology 138:5641-5644 (Pubitemid 27509731)
23. Gómez JM, Maravall FJ, Gómez N, Navarro MA, Casamitjana R, Soler J 2003 Interactions between serum leptin, the insulin-like growth factor-I system, and sex, age, anthropometric and body composition variables in a healthy population randomly selected. J Clin Endocrinol (Oxf) 58:213-219 (Pubitemid 36194277)
24. Vuagnat BA, Pierroz DD, Lalaoui M, Englaro P, Pralong FP, Blum WF, Aubert ML 1998 Evidence for a leptin-neuropeptide Y axis for the regulation of growth hormone secretion in the rat. Neuroendocrinology 67:291-300 (Pubitemid 28230378)
25. Grégoire Nyomba BL, Johnson M, Berard L, Murphy LJ 1999 Relationship between serum leptin and the insulin-like growth factor-I system in humans. Metabolism 48:840-844 (Pubitemid 29310036)
26. Veldhuis JD, Roemmich JN, Richmond EJ, Bowers CY 2006 Somatotropic and gonadotropic axes linkages in infancy, childhood, and the puberty-adult transition. Endocr Rev 27:101-140
27. Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL 1996 Insulin- like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 137:3717-3728 (Pubitemid 26284638)
28. Copeland KC, Kuehl TJ, Castracane VD 1982 Pubertal endocrinology of the baboon: elevated somatomedin-C/insulin-like growth factor I at puberty. J Clin Endocrinol Metab 55:1198-1201 (Pubitemid 13204266)
29. Rosenfield RI, Furlanetto R, Bock D 1983 Relationship of somatomedin- C concentrations to pubertal changes. J Pediatr 103:723-728 (Pubitemid 14235433)
30. Daftary SS, Gore AC 2004 The hypothalamic insulin-like growth factor-1 receptor and its relationship to gonadotropin-releasing hormones neurones during postnatal development. J Neuroendocrinol 16:160-169 (Pubitemid 38256463)
31. Cuttler L, Van Vliet G, Conte FA, Kaplan SL, Grumbach MM 1985 Somatomedin-C levels in children and adolescents with gonadal dysgenesis: differences from age-matched normal females and effect of chronic estrogen replacement therapy. J Clin Endocrinol Metab 60:1087-1092 (Pubitemid 15064763)
32. Wilson ME 1998 Premature elevation in serum insulin-like growth factor-I advances first ovulation in rhesus monkeys. J Endocrinol 158:247-257 (Pubitemid 28342069)
33. Wilson ME, Tanner JM 1994 Somatostatin analog treatment slows growth and the tempo of reproductive maturation in female rhesus monkeys. J Clin Endocrinol Metab 79:495-501 (Pubitemid 24256542)
34. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM 1994 Positional cloning of the mouse obese gene and its human homologue. Nature [Erratum (1995) 374:479] 372:425-432
35. Strobel A, Issad T, Camoin L, Ozata M, Strosberg AD 1998 A leptin missense mutation associated with hypogonadism and morbid obesity. Nat Genet 18:213-215
36. Ozata M, Ozdemir IC, Licinio J 1999 Human leptin deficiency caused by a missense mutation: multiple endocrine defects, decreased sympathetic tone, and immune system dysfunction indicate new targets for leptin action, greater central than peripheral resistance to the effects of leptin, and spontaneous correction of leptinmediated defects. J Clin Endocrinol Metab [Erratum (2000) 85:416] 84:3686-3695
37. Farooqi IS, Wangensteen T, Collins S, Kimber W, Matarese G, Keogh JM, Lank E, Bottomley B, Lopez-Fernandez J, Ferraz-Amaro I, Dattani MT, Ercan O, Myhre AG, Retterstol L, Stanhope R, Edge JA, McKenzie S, Lessan N, Ghodsi M, De Rosa V, Perna F, Fontana S, Barroso I, Undlien DE, O'Rahilly S 2007 Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor. N Engl J Med 356:237-247 (Pubitemid 46143227)
38. Cheung CC, Thornton JE, Kuijper JL, Weigle DS, Clifton DK, Steiner RA 1997 Leptin is a metabolic gate for the onset of puberty in the female rat. Endocrinology 138:855-858 (Pubitemid 27110945)
39. Nagatani S, Guthikonda P, Thompson RC, Tsukamura H, Maeda KI, Foster DL 1998 Evidence for GnRH regulation by leptin: leptin administration prevents reduced pulsatile LH secretion during fasting. Neuroendocrinology 67:370-376 (Pubitemid 28279739)
40. Finn PD, Cunningham MJ, Pau KY, Spies HG, Clifton DK, Steiner RA 1998 The stimulatory effect of leptin on the neuroendocrine reproductive axis of the monkey. Endocrinology 139:4652-4662 (Pubitemid 28487784)
41. Foster DL, Nagatani S 1999 Physiological perspectives on leptin as a regulator of reproduction: role in timing puberty. Biol Reprod 60:205-215 (Pubitemid 29063858)
42. Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL, Clifton DK, Steiner RA 1996 Leptin is a metabolic signal to the reproductive system. Endocrinology 137:3144-3147 (Pubitemid 26193035)
43. Ahima RS, Dushay J, Flier SN, Prabakaran D, Flier JS 1997 Leptin accelerates the onset of puberty in normal female mice. J Clin Invest 99:391-395 (Pubitemid 27414795)
44. Chehab FF, Lim ME, Lu R 1996 Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet 12:318-320 (Pubitemid 26080094)
45. Gruaz NM, Lalaoui M, Pierroz DD, Englaro P, Sizonenko PC, Blum WF, Aubert ML 1998 Chronic administration of leptin into the lateral ventricle induces sexual maturation in severely food-restricted female rats. J Neuroendocrinol 10:627-633 (Pubitemid 28347246)
46. Nagatani S, Zeng Y, Keisler DH, Foster DL, Jaffe CA 2000 Leptin regulates pulsatile luteinizing hormone and growth hormone secretion in the sheep. Endocrinology 141:3965-3975
47. Ahima RS, Prabakaran D, Flier JS 1998 Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 101:1020-1027 (Pubitemid 28125280)
48. Mantzoros CS, Flier JS, Rogol AD 1997 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 82:1066-1070 (Pubitemid 27166643)
49. Matkovic V, Ilich JZ, Skugor M, Badenhop NE, Goel P, Clairmont A, Klisovic D, Nahhas RW, Landoll JD 1997 Leptin is inversely related to age at menarche in human females. J Clin Endocrinol Metab 82:3239-3245 (Pubitemid 27419064)
50. Carlsson B, Ankarberg C, Rosberg S, Norjavaara E, Albertsson- Wikland K, Carlsson LM 1997 Serum leptin concentrations in relation to pubertal development. Arch Dis Child 77:396-400
51. Palmert MR, Radovick S, Boepple PA 1998 Leptin levels in children with central precocious puberty. J Clin Endocrinol Metab 83:2260-2265 (Pubitemid 28503011)
52. Horlick MB, Rosenbaum M, Nicolson M, Levine LS, Fedun B, Wang J, Pierson Jr RN, Leibel RL 2000 Effect of puberty on the relationship between circulating leptin and body composition. J Clin Endocrinol Metab 85:2509-2518 (Pubitemid 32269209)
53. Ankarberg-Lindgren C, Dahlgren J, Carlsson B, Rosberg S, Carlsson L, Wikland KA, Norjavaara E 2001 Leptin levels show diurnal variation throughout puberty in healthy children, and follow a gender-specific pattern. Eur J Endocrinol 145:43-51 (Pubitemid 32677675)
54. Garcia-Mayor RV, Andrade MA, Rios M, Lage M, Dieguez C, Casanueva FF 1997 Serum leptin levels in normal children: relationship to age, gender, body mass index, pituitary-gonadal hormones, and pubertal stage. J Clin Endocrinol Metab 82:2849-2855 (Pubitemid 27385638)
55. Ahmed ML, Ong KK, Watts AP, Morrell DJ, Preece MA, Dunger DB 2001 Elevated leptin levels are associated with excess gains in fat mass in girls, but not boys, with type 1 diabetes: longitudinal study during adolescence. J Clin Endocrinol Metab 86:1188-1193 (Pubitemid 32323003)
56. Plant TM, Durrant AR 1997 Circulating leptin does not appear to provide a signal for triggering the initiation of puberty in the male rhesus monkey (Macaca mulatta). Endocrinology 138:4505-4508 (Pubitemid 27408504)
57. Urbanski HF, Pau KY 1998 A biphasic developmental pattern of circulating leptin in the male rhesus macaque (Macaca mulatta). Endocrinology 139:2284-2286 (Pubitemid 28513749)
58. Mann DR, Akinbami MA, Gould KG, Castracane VD 2000 A longitudinal study of leptin during development in the male rhesus monkey: the effect of body composition and season on circulating leptin levels. Biol Reprod 62:285-291 (Pubitemid 30067327)
59. Plant TM 2001 Leptin, growth hormone, and the onset of primate puberty. J Clin Endocrinol Metab 86:458-460 (Pubitemid 32109837)
60. Mann DR, Bhat GK, Ramaswamy S, Stah CD, Plant TM 2007 Regulation of circulating leptin and its soluble receptor during pubertal development in the male rhesus monkey (Macaca mulatta). Endocrine 31:125-129 (Pubitemid 350195145)
61. Barker-Gibb ML, Sahu A, Pohl CR, Plant TM 2002 Elevating circulating leptin in prepubertal male rhesus monkeys (Macaca mulatta) does not elicit precocious gonadotropin-releasing hormone release, assessed indirectly. J Clin Endocrinol Metab 87:4976-4983 (Pubitemid 35316335)
62. Suter KJ, Pohl CR, Wilson ME 2000 Circulating concentrations of nocturnal leptin, growth hormone, and insulin-like growth factor-I increase before the onset of puberty in agonadal male monkeys: potential signals for the initiation of puberty. J Clin Endocrinol Metab 85:808-814 (Pubitemid 32273672)
63. Vong L, Ye C, Yang Z, Choi B, Chua Jr S, Lowell BB 2011 Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154
64. Mitsushima D, Hei DL, Terasawa E 1994 GABA is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci USA 91:395-399
65. Terasawa E, Luchansky LL, Kasuya E, Nyberg CL 1999 An increase in glutamate release follows a decrease in gamma-aminobutyric acid (GABA) and the pubertal increase in LHRH release in female rhesus monkeys. J Neuroendocrinol 11:275-282 (Pubitemid 29149881)
66. Terasawa E, Fernandez DL 2001 Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 22:111-151 (Pubitemid 32187805)
67. Roa J, Tena-Sempere M 2010 Energy balance and puberty onset: emerging role of central mTOR signaling. Trends Endocrinol Metab 21:519-528
68. George JT, Millar RP, Anderson RA 2010 Hypothesis: kisspeptin mediates male hypogonadism in obesity and type 2 diabetes. Neuroendocrinology 91:302-307
69. Donato Jr J, Cravo RM, Frazão R, Gautron L, Scott MM, Lachey J, Castro IA, Margatho LO, Lee S, Lee C, Richardson JA, Friedman J, Chua Jr S, Coppari R, Zigman JM, Elmquist JK, Elias CF 2011 Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons. J Clin Invest 121:355-368
70. Morley TP 1954 Hypothalamic tumor and precocious puberty. J Clin Endocrinol Metab 14:1
71. Byrnes ND, Cloutier MD, Hayles AB 1974 The central nervous system and precocious puberty. In: Grumbach MM, Grave GD, Mayer FE, eds. The control of the onset of puberty. New York: Wiley and Sons; 213
72. Siegel-Witchel S 1995 CNS lesions, neurologic disorders, and puberty in man. In: Plant TM, Lee PA, eds. The neurobiology of puberty. Bristol, UK: Journal of Endocrinology Ltd.; 229-239