Developmentally delimited emergence of more orderly luteinizing hormone and testosterone secretion during late prepuberty in boys
- PMID: 11231982
- DOI: 10.1210/jcem.86.1.7127
Developmentally delimited emergence of more orderly luteinizing hormone and testosterone secretion during late prepuberty in boys
Abstract
To quantitate changing feedback control in the GnRH-LH/FSH-testosterone axis in male puberty, we here quantitate the orderliness of hormone release patterns using the regularity (pattern-sensitive) statistic, approximate entropy (ApEn), in 46 eugonadal boys representing 6 genitally defined stages of normal puberty. ApEn is a single variable, model-free, and scale-independent barometer of coordinate signaling or integrative regulation within a coupled neuroendocrine axis. Accordingly, we quantitated ApEn of LH profiles obtained by immunofluorometric assay of sera sampled every 20 min for 24 h. LH ApEn declined remarkably between early prepuberty (genital stage I-A: mean bone age, 4.6 +/- 1.6 yr; testis volume, <3 mL for at least 3 succeeding yr) and late prepuberty (genital stage I-C: bone age, 8.7 +/- 1.8 yr; testis volume, <3 mL for up to 1 yr thereafter; P: = 0.00019), which indicates the acquisition of more regular LH release patterns in late prepuberty. Maximal LH orderliness occurred in puberty stage II (bone age, 10.7 +/- 1.0 yr; testis volume, 2.8 +/- 0.4 mL). The LH secretory process was more disorderly in mid- and later puberty (Tanner stages III and IV). Transpubertal variations in testosterone ApEn manifested a similar tempo, i.e. the greatest regularity of testosterone secretion (lowest ApEn) emerged in Tanner genital stage II (P: < 10(-)(7)), with less orderly patterns evident both earlier and later in sexual development. In contrast, FSH ApEn values remained invariant of pubertal status. Analysis of bihormonal coupling using the theoretically related bivariate cross-ApEn statistic disclosed maximal 2-hormone synchrony for LH and testosterone secretion in genital stage II (P: = 0.031), with relative deterioration of coordinate LH and testosterone release patterns both before and after. LH and FSH release became maximally synchronous at the end of prepuberty (genital stage I-C; P: = 0.029), and FSH and testosterone synchrony peaked in pubertal stage III (P: = 0.037). As mean 24-h serum concentrations of LH, FSH, and testosterone rose transpubertally by 35-fold (LH), 68-fold (FSH), and 70-fold (testosterone), respectively, we infer that pubertal developmental stage per se rather than level of hormone output dictates coordinate GnRH-LH/FSH-testosterone secretion. In summary, in eugonadal boys, the regularity of 24-h LH and testosterone secretory patterns undergoes well defined pubertal stage-specific control. No sexually developmentally delimited regulation is inferable for FSH. The concept of temporally biphasic puberty-dependent variations in neurohormone secretory regularity contrasts with the unidirectional rise in daily hormone output. Accordingly, we infer that late prepuberty and early puberty (Tanner genital stages IC and II) embody a physiologically unique sexual developmental window, marked by transiently enhanced LH and testosterone feedback stability in boys. Whether analogous plasticity of hypothalamo-pituitary-gonadal interactions unfolds during female adolescence is not known.
Similar articles
-
Disruption of the joint synchrony of luteinizing hormone, testosterone, and androstenedione secretion in adolescents with polycystic ovarian syndrome.J Clin Endocrinol Metab. 2001 Jan;86(1):72-9. doi: 10.1210/jcem.86.1.7125. J Clin Endocrinol Metab. 2001. PMID: 11231981
-
Disruption of the young-adult synchrony between luteinizing hormone release and oscillations in follicle-stimulating hormone, prolactin, and nocturnal penile tumescence (NPT) in healthy older men.J Clin Endocrinol Metab. 1999 Oct;84(10):3498-505. doi: 10.1210/jcem.84.10.6100. J Clin Endocrinol Metab. 1999. PMID: 10522986
-
Novel modalities for appraising individual and coordinate pulsatile hormone secretion: the paradigm of luteinizing hormone and testosterone release in the aging male.Mol Psychiatry. 1997 Jan;2(1):70-80. doi: 10.1038/sj.mp.4000232. Mol Psychiatry. 1997. PMID: 9154220 Review.
-
Neuroendocrine mechanisms mediating awakening of the human gonadotropic axis in puberty.Pediatr Nephrol. 1996 Jun;10(3):304-17. doi: 10.1007/BF00866767. Pediatr Nephrol. 1996. PMID: 8792395 Review.
-
Ontogeny of gonadotropin, testosterone, and inhibin secretion in normal boys through puberty based on overnight serial sampling.J Clin Endocrinol Metab. 1995 Jul;80(7):2046-52. doi: 10.1210/jcem.80.7.7608253. J Clin Endocrinol Metab. 1995. PMID: 7608253
Cited by
-
In early pubertal boys, testosterone and LH are associated with improved anti-oxidation during an aerobic exercise bout.Endocrine. 2019 Nov;66(2):370-380. doi: 10.1007/s12020-019-02037-1. Epub 2019 Aug 4. Endocrine. 2019. PMID: 31378848
-
Interrelations among the adipocytokines leptin and adiponectin, oxidative stress and aseptic inflammation markers in pre- and early-pubertal normal-weight and obese boys.Endocrine. 2017 Mar;55(3):925-933. doi: 10.1007/s12020-017-1227-3. Epub 2017 Jan 16. Endocrine. 2017. PMID: 28092067
-
Age-related responses in circulating markers of redox status in healthy adolescents and adults during the course of a training macrocycle.Oxid Med Cell Longev. 2015;2015:283921. doi: 10.1155/2015/283921. Epub 2015 Apr 6. Oxid Med Cell Longev. 2015. PMID: 25945150 Free PMC article.
-
Antioxidation improves in puberty in normal weight and obese boys, in positive association with exercise-stimulated growth hormone secretion.Pediatr Res. 2015 Aug;78(2):158-64. doi: 10.1038/pr.2015.85. Epub 2015 May 4. Pediatr Res. 2015. PMID: 25938733
-
Developmental and contextual considerations for adrenal and gonadal hormone functioning during adolescence: Implications for adolescent mental health.Dev Psychobiol. 2015 Sep;57(6):742-68. doi: 10.1002/dev.21214. Epub 2014 Apr 11. Dev Psychobiol. 2015. PMID: 24729154 Free PMC article. Review.
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Medical
Research Materials