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Influences on the Onset and Tempo of Puberty in Human Beings And

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Influences on the Onset and Tempo of Puberty in Human Beings And Hormones and Behavior 64 (2013) 250–261 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh Review Influences on the onset and tempo of puberty in human beings and implications for adolescent psychological development Yvonne Lee ⁎, Dennis Styne University of California Davis Medical Center, 2516 Stockton Boulevard, Ticon II, Sacramento, CA 95817, USA article info abstract Keywords: This article is part of a Special Issue “Puberty and Adolescence”. Secular trends in puberty Influences on temp of puberty Historical records reveal a secular trend toward earlier onset of puberty in both males and females, often attrib- Endocrine disrupting chemicals uted to improvements in nutrition and health status. The trend stabilized during the mid 20th century in many countries, but recent studies describe a recurrence of a decrease in age of pubertal onset. There appears to be an associated change in pubertal tempo in girls, such that girls who enter puberty earlier have a longer duration of puberty. Puberty is influenced by genetic factors but since these effects cannot change dramatically over the past century, environmental effects, including endocrine disrupting chemicals (EDCs), and perinatal conditions offer alternative etiologies. Observations that the secular trends in puberty in girls parallel the obesity epidemic provide another plausible explanation. Early puberty has implications for poor behavioral and psychosocial out- comes as well as health later in life. Irrespective of the underlying cause of the ongoing trend toward early puber- ty, experts in the field have debated whether these trends should lead clinicians to reconsider a lower age of normal puberty, or whether such a new definition will mask a pathologic etiology. © 2013 Elsevier Inc. All rights reserved. Contents Introduction ................................................................ 251 Developmental stages of the control of puberty ................................................ 251 Hypothalamic–pituitary–gonadal axis .................................................. 251 Fetal Life ............................................................... 251 Prepuberty and puberty ........................................................ 251 Physical changes associated with puberty .................................................. 251 Body composition changes with puberty ................................................... 252 Determining onset of puberty ........................................................ 252 Females ................................................................ 252 Males ................................................................. 252 Secular trends in puberty .......................................................... 252 Females ................................................................ 252 Males ................................................................. 253 The tempo of puberty ............................................................ 253 Influences on onset and tempo of puberty .................................................. 253 Genetic effects on puberty and menarche ................................................ 253 Weight and nutrition .......................................................... 254 Ethnic differences ........................................................... 254 Stress ................................................................. 254 Perinatal influences and the fetal origins of adult disease ........................................... 254 Environmental endocrine disruptors and puberty ............................................... 255 Sources of EDCs ............................................................ 255 Dioxin and dioxin-like compounds ................................................... 255 Halogenated aromatic compounds .................................................... 255 ⁎ Corresponding author. Fax: +1 916 734 7070. E-mail address: [email protected] (Y. Lee). 0018-506X/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yhbeh.2013.03.014 Y. Lee, D. Styne / Hormones and Behavior 64 (2013) 250–261 251 Organochlorines ............................................................ 256 Endosulfans .............................................................. 257 Lead ................................................................. 257 Barriers to understanding the effect of EDCs on human population .................................... 257 Neurodevelopmental consequences of EDCs ............................................... 257 Clinical consequences ........................................................... 257 Premature puberty ........................................................... 257 Conclusions ................................................................ 258 References ................................................................. 258 Introduction several hours thereafter. As pubertal development progresses, the peaks of serum LH and FSH occur more often during waking hours; Puberty is best considered one stage in the continuum of repro- and, finally, in late puberty, the peaks occur at all times, eliminating ductive life rather than a single event (Styne and Grumbach, 2011). the diurnal variation (Styne and Grumbach, 2011). Thus, changes that begin during fetal life result in the maturation of The development of reproduction is essential to a species and the hypothalamic–pituitary–gonadal (HPG) axis, a process that in- thus duplicate and complex mechanisms ensure this progression. cludes suppression and then re-activation of the hypothalamic go- While investigators are making progress in uncovering the control nadotropin releasing hormone (GnRH) pulse generator, enhanced of the onset of puberty, much remains to be done. Genes coding for gonadotropin secretion and gonadal maturation with reproductive transcription factors such as CLOCK and BMAL1 regulate cellular function. rhythms that are involved in the control of puberty (Tolson and Chappell, 2012). Kisspeptin, encoded by the KiSS-1 gene, is implicat- Developmental stages of the control of puberty ed as a major “gatekeeper” of GnRH function. Kisspeptins activate a G protein coupled receptor, GPR54, encoded by the KISS1R gene, that is Hypothalamic–pituitary–gonadal axis expressed in the brain, pituitary, placenta and on GnRH neurons. Many lines of evidence suggest that KiSS-1 gene regulates puberty Pituitary gonadotropin secretion is controlled by the hypothala- at the level of the GnRH pulse generator (Tolson and Chappell, mus, which releases pulses of GnRH into the pituitary–portal system 2012). While GnRH content remains relatively constant during to stimulate the anterior pituitary gland to episodically release go- puberty, hypothalamic kisspeptin levels rise (Tolson and Chappell, nadotropins (Styne and Grumbach, 2011). Control of GnRH secretion 2012). Loss of function of the GPR54 gene results in idiopathic is exerted by a “hypothalamic pulse generator” in the arcuate nucleus hypogonadotrophic hypogonadism (de Roux et al., 2003; Seminara which is responsive to higher central nervous system (CNS) centers et al., 2003), while over expression of GPR54 or Kisspeptin leads and sensitive to feedback control from gonadal secretory products. to precocious puberty (Teles et al., 2011). More on the regula- In males, LH stimulates the Leydig cells to secrete testosterone, tory role of kisspeptins can be found in another article within this and FSH stimulates the Sertoli cells to produce inhibin which exerts issue of Hormones and Behavior (Sanchez-Garrido MA and Tana- feedback on the hypothalamic–pituitary axis to inhibit FSH. In females, Sempere M). FSH stimulates the granulosa cells to produce estrogen and the follicles to secrete inhibin. LH appears to play a minor role in the endocrine milieu until menarche, at which point it triggers ovulation and Physical changes associated with puberty later stimulates the theca cells to secrete androgens. Secondary sexual maturation and endocrine changes during pu- Fetal Life bertal development include thelarche, gonadarche, pubarche, and adrenarche. Increased growth rate is one of the first signs of puberty During fetal life, GnRH content in the hypothalamus and gonadotro- and peak height velocity (PHV) occurs relatively early in female pu- pin content in the pituitary gland increase, pulsatile release of GnRH berty (Tanner and Davies, 1985). Thelarche, the onset of breast devel- and gonadotropins develops and rise until midgestation (Styne, 2011; opment, is caused by an increase in the secretion of ovarian estrogen Styne and Grumbach, 2011). After midgestation, GnRH release de- and is often the first sign of puberty noted in girls during routine creases, due to CNS inhibition, which leads to decreased gonadotropin evaluations (Styne, 2011). Isolated premature thelarche may occur secretion; elevated maternal estrogens also suppress gonadotropin se- unrelated to normal GnRH dependent puberty. Gonadarche marks cretion until term. Once maternal estrogen has been cleared, postnatal the increase in sex steroid secretion from the gonads under the con- peaks of serum LH and FSH occur for more than 6 months after birth trol of the hypothalamic pituitary axis; in boys, gonadarche is associ- (Grumbach, 2002). During the juvenile pause, the period between infan- ated with increased testicular volume (Styne, 2011). The maturation cy and the peripubertal period, basal and GnRH
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