Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents
Parent, Anne-Simone ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Franssen, Delphine ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
FUDVOYE, Julie ; Centre Hospitalier Universitaire de Liège - CHU > pédiatrie
GERARD, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Pédiatrie
Bourguignon, Jean-Pierre ; Université de Liège - ULiège > Département des sciences cliniques > Pédiatrie
Language :
English
Title :
Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents
Abreu A.P., et al. Central precocious puberty caused by mutations in the imprinted gene MKRN3. N. Engl. J. Med. 2013, 368(26):2467-2475.
Adair L.S. Size at birth predicts age at menarche. Pediatrics 2001, 107(4):E59.
Adewale H.B., et al. Neonatal bisphenol-a exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol. Reprod. 2009, 81(4):690-699.
Adgent M.A., et al. Early-life soy exposure and age at menarche. Paediatr. Perinat. Epidemiol. 2012, 26(2):163-175.
Aksglaede L., et al. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics 2009, 123(5):e932-e939.
Aksglaede L., et al. Age at puberty and the emerging obesity epidemic. PLoS One 2009, 4(12):e8450.
Ashby J., et al. Normal sexual development of rats exposed to butyl benzyl phthalate from conception to weaning. Regul. Toxicol. Pharmacol. 1997, 26(1 Pt 1):102-118.
Ashby J., Lefevre P.A. The peripubertal male rat assay as an alternative to the Hershberger castrated male rat assay for the detection of anti-androgens, oestrogens and metabolic modulators. J. Appl. Toxicol. 2000, 20(1):35-47.
Barbarino A., et al. Corticotropin-releasing hormone inhibition of gonadotropin secretion during the menstrual cycle. Metabolism 1989, 38(6):504-506.
Barker D.J., Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1986, 1(8489):1077-1081.
Bateman H.L., Patisaul H.B. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased GnRH activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 2008, 29(6):988-997.
Bethea C.L., Centeno M.L., Cameron J.L. Neurobiology of stress-induced reproductive dysfunction in female macaques. Mol. Neurobiol. 2008, 38(3):199-230.
Biro F.M., et al. Onset of breast development in a longitudinal cohort. Pediatrics 2013, 132(6):1019-1027.
Biro F.M., Khoury P., Morrison J.A. Influence of obesity on timing of puberty. Int. J. Androl. 2006, 29(1):272-277. (discussion 286-90).
Boersma G.J., et al. Prenatal stress decreases Bdnf expression and increases methylation of exon IV in rats. Epigenetics 2013, 9(3).
Botelho G.G., et al. Reproductive effects of di(2-ethylhexyl)phthalate in immature male rats and its relation to cholesterol, testosterone, and thyroxin levels. Arch. Environ. Contam. Toxicol. 2009, 57(4):777-784.
Boukouvalas G., et al. Post weaning high fat feeding affects rats' behavior and hypothalamic pituitary adrenal axis at the onset of puberty in a sexually dimorphic manner. Neuroscience 2008, 153(2):373-382.
Bouret S.G. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 2004, 304(5667):108-110.
Bouret, S.G. et al., 2007. Impact of neonatal nutrition on development of brain metabolic circuits in mice. Soc Neurosci Abstr. 33:33:300.21/VV8.
Bourguignon J.P., et al. Maturation of the hypothalamic control of pulsatile gonadotropin-releasing hormone secretion at onset of puberty. I. Increased activation of N-methyl-D-aspartate receptors. Endocrinology 1990, 127(2):873-881.
Bourguignon J.P., et al. Neuroendocrine mechanism of onset of puberty. Sequential reduction in activity of inhibitory and facilitatory N-methyl-D-aspartate receptors. J. Clin. Invest. 1992, 90(5):1736-1744.
Bourguignon J.P., et al. Early neuroendocrine disruption in hypothalamus and hippocampus: developmental effects including female sexual maturation and implications for endocrine disrupting chemical screening. J. Neuroendocrinol. 2013, 25(11):1079-1087.
Bourguignon J.P., Franchimont P. Puberty-related increase in episodic LHRH release from rat hypothalamus in vitro. Endocrinology 1984, 114(5):1941-1943.
Bourguignon J.P., et al. Changes in pubertal timing: past views, recast issues. Brain Crosstalk in Puberty and Adolescence 2015, 160-172. Springer, Switzerland. J.P. Bourguignon, J.C. Carel, Y. Christen (Eds.).
Brüning J.C., et al. Role of brain insulin receptor in control of body weight and reproduction. Science 2000, 289(5487):2122-2125.
Burcelin R., et al. Gonadotropin-releasing hormone secretion from hypothalamic neurons: stimulation by insulin and potentiation by leptin. Endocrinology 2003, 144(10):4484-4491.
Burroughs C.D., Bern H.A., Stokstad E.L. Prolonged vaginal cornification and other changes in mice treated neonatally with coumestrol, a plant estrogen. J. Toxicol. Environ. Health 1985, 15(1):51-61.
Burton P.J., Waddell B.J. Dual function of 11beta-hydroxysteroid dehydrogenase in placenta: modulating placental glucocorticoid passage and local steroid action. Biol. Reprod. 1999, 60(2):234-240.
Campfield L.A., et al. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 1995, 269(5223):546-549.
Caron E., et al. Alteration in neonatal nutrition causes perturbations in hypothalamic neural circuits controlling reproductive function. J. Neurosci. 2012, 32(33):11486-11494.
Castellano J.M., et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 2005, 146(9):3917-3925.
Castellano J.M., et al. Kisspeptins: bridging energy homeostasis and reproduction. Brain Res. 2010, 1364:129-138.
Castellano J.M., et al. Early metabolic programming of puberty onset: impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology 2011, 152(9):3396-3408.
Cates P.S., Li X.F., O'Byrne K.T. The influence of 17beta-oestradiol on corticotrophin-releasing hormone induced suppression of luteinising hormone pulses and the role of CRH in hypoglycaemic stress-induced suppression of pulsatile LH secretion in the female rat. Stress 2004, 7(2):113-118.
Ceccatelli R., et al. Gene expression and estrogen sensitivity in rat uterus after developmental exposure to the polybrominated diphenylether PBDE 99 and PCB. Toxicology 2006, 220(2-3):104-116.
Cheng G., et al. Beyond overweight: nutrition as an important lifestyle factor influencing timing of puberty. Nutr. Rev. 2012, 70(3):133-152.
Chernoff N., et al. Reproductive effects of maternal and pre-weaning undernutrition in rat offspring: age at puberty, onset of female reproductive senescence and intergenerational pup growth and viability. Reprod. Toxicol. 2009, 28(4):489-494.
Clancy B., et al. Extrapolating brain development from experimental species to humans. Neurotoxicology 2007, 28(5):931-937.
Clarke I.J., et al. Evidence that RF-amide related peptides are inhibitors of reproduction in mammals. Front. Neuroendocrinol. 2009, 30(3):371-378.
Clavel-Chapelon F., E3N-EPIC group Evolution of age at menarche and at onset of regular cycling in a large cohort of French women. Hum. Reprod. 2002, 17(1):228-232.
Connor K.L., et al. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J. Physiol. 2012, 590(Pt 9):2167-2180.
Cooper C., et al. Childhood growth and age at menarche. Br. J. Obstet. Gynaecol. 1996, 103(8):814-817.
da Silva Faria, T., da Fonte Ramos C., Sampaio F.J. Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. J. Nutr. Biochem. 2004, 15(2):123-127.
Dacou-Voutetakis C., Karidis N. Congenital adrenal hyperplasia complicated by central precocious puberty: treatment with LHRH-agonist analogue. Ann. N. Y. Acad. Sci. 1993, 687(1):250-254.
de Ridder C.M., et al. Body fat mass, body fat distribution, and pubertal development: a longitudinal study of physical and hormonal sexual maturation of girls. J. Clin. Endocrinol. Metab. 1992, 75(2):442-446.
de Roux N., et al. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. USA 2003, 100(19):10972-10976.
den Hoed M., et al. Genetic susceptibility to obesity and related traits in childhood and adolescence: influence of loci identified by genome-wide association studies. Diabetes 2010, 59(11):2980-2988.
Den Hond E., et al. Sexual maturation in relation to polychlorinated aromatic hydrocarbons: Sharpe and Skakkebaek's hypothesis revisited. Environ. Health Perspect. 2002, 110(8):771-776.
Den Hond E., et al. Internal exposure to pollutants and sexual maturation in Flemish adolescents. J. Expo. Sci. Environ. Epidemiol. 2011, 21(3):224-233.
Deng F., et al. Effects of growth environments and two environmental endocrine disruptors on children with idiopathic precocious puberty. Eur. J. Endocrinol. 2012, 166(5):803-809.
Denham M., et al. Relationship of lead, mercury, mirex, dichlorodiphenyldichloroethylene, hexachlorobenzene, and polychlorinated biphenyls to timing of menarche among Akwesasne Mohawk girls. Pediatrics 2005, 115(2):e127-e134.
Dolinoy D.C., Weidman J.R., Jirtle R.L. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod. Toxicol. 2007, 23(3):297-307.
Donato J., et al. 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. 2011, 121(1):355-368.
dos Santos Silva I., et al. Prenatal factors, childhood growth trajectories and age at menarche. Int. J. Epidemiol. 2002, 31(2):405-412.
Ducharme J.R., Collu R. Pubertal development: normal, precocious and delayed. Clin. Endocrinol. Metab. 1982, 11(1):57-87.
Dunger D.B., Ahmed M.L., Ong K.K. Early and late weight gain and the timing of puberty. Mol. Cell. Endocrinol. 2006, 254-255:140-145.
Elks C.E., et al. Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat. Genet. 2010, 42(12):1077-1085.
Ellinwood W.E., Baughman W.L., Resko J.A. The effects of gonadectomy and testosterone treatment on luteinizing hormone secretion in fetal rhesus monkeys. Endocrinology 1982, 110(1):183-189.
Ellis B.J. Timing of pubertal maturation in girls: an integrated life history approach. Psychol. Bull. 2004, 130(6):920-958.
Ellison P.T. Skeletal growth, fatness and menarcheal age: a comparison of two hypotheses. Hum. Biol. 1982, 54(2):269-281.
Engelbregt M.J., et al. The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr. Res. 2000, 48(6):803-807.
Engelbregt M.J., et al. Body composition and bone measurements in intra-uterine growth retarded and early postnatally undernourished male and female rats at the age of 6months: comparison with puberty. Bone 2004, 34(1):180-186.
Fernandez M., et al. Neonatal exposure to bisphenol a alters reproductive parameters and gonadotropin releasing hormone signaling in female rats. Environ. Health Perspect. 2009, 117(5):757-762.
Fernandez M., et al. Neonatal exposure to bisphenol a and reproductive and endocrine alterations resembling the polycystic ovarian syndrome in adult rats. Environ. Health Perspect. 2010, 118(9):1217-1222.
Fernandez-Rhodes L., et al. Association of adiposity genetic variants with menarche timing in 92,105 women of European descent. Am. J. Epidemiol. 2013, 178(3):451-460.
Forbes S., et al. Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamicmedial preoptic area and pulsatile luteinizing hormone secretion in the female rat. Neurosci. Lett. 2006, 147(1):510-519.
Foster D.L., Yellon S.M., Olster D.H. Internal and external determinants of the timing of puberty in the female. J. Reprod. Fertil. 1985, 75(1):327-344.
Franssen D., Ioannou Y.S., et al. Pubertal timing after neonatal diethylstilbestrol exposure in female rats: neuroendocrine versus peripheral effects and additive role of prenatal food restriction. Reprod. Toxicol. 2013.
Fraser M.O., Arslan M., Plant T.M. Androgen and estrogen treatment, alone or in combination, differentially influences bone maturation and hypothalamic mechanisms that time puberty in the male rhesus monkey (Macaca mulatta). Pediatr. Res. 2005, 57(1):141-148.
Frisch R.E., Revelle R. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science 1970, 169(3943):397-399.
Fungfuang W., et al. Early onset of reproductive function in female rats treated with a high-fat diet. J. Vet. Med. Sci. 2013, 75(4):523-526.
Ge R.S., et al. Biphasic effects of postnatal exposure to diethylhexylphthalate on the timing of puberty in male rats. J. Androl. 2007, 28(4):513-520.
Gellert R.J., Heinrichs W.L., Swerdloff R.S. DDT homologues: estrogen-like effects on the vagina, uterus and pituitary of the rat. Endocrinology 1972, 91(4):1095-1100.
Gellert R.J., Heinrichs W.L., Swerdloff R. Effects of neonatally-administered DDT homologs on reproductive function in male and female rats. Neuroendocrinology 1974, 16(2):84-94.
Gereltsetseg G., et al. Delay in the onset of puberty of intrauterine growth retarded female rats cannot be rescued with hypernutrition after birth. Endocr. J. 2012, 59(11):963-972.
Giampietro P.G., et al. Soy protein formulas in children: no hormonal effects in long-term feeding. J. Pediatr. Endocrinol. Metab. 2004, 17(2):191-196.
Gladen B.C., Ragan N.B., Rogan W.J. Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J. Pediatr. 2000, 136(4):490-496.
Goldstein J.R. A secular trend toward earlier male sexual maturity: evidence from shifting ages of male young adult mortality. PLoS One 2011, 6(8):e14826.
Goy R.W., Bercovitch F.B., McBrair M.C. Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm. Behav. 1988, 22(4):552-571.
Grandjean P., et al. Reproductive hormone profile and pubertal development in 14-year-old boys prenatally exposed to polychlorinated biphenyls. Reprod. Toxicol. 2012, 34(4):498-503.
Gray L.E., Laskey J., OstbyGray J. Chronic di-n-butyl phthalate exposure in rats reduces fertility and alters ovarian function during pregnancy in female Long Evans hooded rats. Toxicol. Sci. 2006, 93(1):189-195.
Grumbach M.M. The neuroendocrinology of human puberty revisited. Horm. Res. 2002, 57(Suppl. 2):2-14.
Guo Y.L., et al. Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int. Arch. Occup. Environ. Health 2004, 77(3):153-158.
Guzman C., et al. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J. Physiol. 2006, 572(Pt 1):97-108.
He C., et al. Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat. Genet. 2009, 41(6):724-728.
He Q., Karlberg J. Bmi in childhood and its association with height gain, timing of puberty, and final height. Pediatr. Res. 2001, 49(2):244-251.
Heinrichs W.L., et al. DDT administered to neonatal rats induces persistent estrus syndrome. Science 1971, 173(3997):642-643.
Herman R.A., Zehr J.L., Wallen K. Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys. Psychoneuroendocrinology 2006, 31(1):118-130.
Herman-Giddens M.E., et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics 1997, 99(4):505-512.
Herman-Giddens M.E., et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics 2012, 130(5):e1058-e1068.
Himes J.H. Examining the evidence for recent secular changes in the timing of puberty in US children in light of increases in the prevalence of obesity. Mol. Cell. Endocrinol. 2006, 254-255:13-21.
Holly J.M., et al. Relationship between the pubertal fall in sex hormone binding globulin and insulin-like growth factor binding protein-I. A synchronized approach to pubertal development?. Clin. Endocrinol. 1989, 31(3):277-284.
Honma S., et al. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod. Toxicol. 2002, 16(2):117-122.
Howdeshell K.L., et al. Exposure to bisphenol A advances puberty. Nature 1999, 401(6755):763-764.
Howerton C.L., Bale T.L. Prenatal programing: at the intersection of maternal stress and immune activation. Horm. Behav. 2012, 62(3):237-242.
Hu J., et al. Short-term neonatal/prepubertal exposure of dibutyl phthalate (DBP) advanced pubertal timing and affected hypothalamic kisspeptin/GPR54 expression differently in female rats. Toxicology 2013, 314(1):65-75.
Ibanez L., et al. Endocrinology and gynecology of girls and women with low birth weight. Fetal Diagn. Ther. 2011, 30(4):243-249.
Ibanez L., Jimenez R., de Zegher F. Early puberty-menarche after precocious pubarche: relation to prenatal growth. Pediatrics 2006, 117(1):117-121.
Iqbal J., et al. Effects of central infusion of ghrelin on food intake and plasma levels of growth hormone, luteinizing hormone, prolactin, and cortisol secretion in sheep. Endocrinology 2006, 147(1):510-519.
Iwasa T., et al. Effects of intrauterine undernutrition on hypothalamic Kiss1 expression and the timing of puberty in female rats. J. Physiol. 2010, 588(Pt 5):821-829.
Jaquet D., et al. High serum leptin concentrations during catch-up growth of children born with intrauterine growth retardation. J. Clin. Endocrinol. Metab. 1999, 84(6):1949-1953.
Jasoni C.L., et al. Expression of mRNAs encoding receptors that mediate stress signals in gonadotropin-releasing hormone neurons of the mouse. Neuroendocrinology 2005, 82(5-6):320-328.
Jefferson W.N., et al. Oral exposure to genistin, the glycosylated form of genistein, during neonatal life adversely affects the female reproductive system. Environ. Health Perspect. 2009, 117(12):1883-1889.
Jefferson W.N., Padilla-Banks E., Newbold R.R. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol. Reprod. 2005, 73(4):798-806.
Jeurissen A. Age of the establishment of the menarche and its evolution in Belgium during the last 40years. Acta Paediatr. Belg. 1969, 23(6):319-330.
Kaplowitz P.B., et al. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 2001, 108(2):347-353.
Kato H., et al. Effects of bisphenol A given neonatally on reproductive functions of male rats. Reprod. Toxicol. 2006, 22(1):20-29.
Kim H.S., et al. Evaluation of the 20-day pubertal female assay in Sprague-Dawley rats treated with DES, tamoxifen, testosterone, and flutamide. Toxicol. Sci. 2002, 67(1):52-62.
Kim J., et al. High serum isoflavone concentrations are associated with the risk of precocious puberty in Korean girls. Clin. Endocrinol. (Oxf.) 2011, 75(6):831-835.
Kinsey-Jones J.S., et al. Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinising hormone secretion in the female rat. J. Neuroendocrinol. 2009, 21(1):20-29.
Kinsey-Jones J.S., et al. Corticotrophin-releasing factor alters the timing of puberty in the female rat. J. Neuroendocrinol. 2010, 22(2):102-109.
Kirby E.D., et al. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc. Natl. Acad. Sci. USA 2009, 106(27):11324-11329.
Klentrou P., Plyley M. Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls. Br. J. Sports Med. 2003, 37(6):490-494.
Kosut S.S., et al. Prenatal androgens time neuroendocrine puberty in the sheep: effect of testosterone dose. Endocrinology 1997, 138(3):1072-1077.
Kouki T., et al. Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrous cycle and lordosis. Horm. Behav. 2003, 44(2):140-145.
Kouki T., et al. Suppressive effect of neonatal treatment with a phytoestrogen, coumestrol, on lordosis and estrous cycle in female rats. Brain Res. Bull. 2005, 64(5):449-454.
Krstevska-Konstantinova M., et al. Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum. Reprod. 2001, 16(5):1020-1026.
Laws S.C., et al. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol. Sci. 2000, 54(1):154-167.
Laws S.C., et al. Effects of altered food intake during pubertal development in male and female wistar rats. Toxicol. Sci. 2007, 100(1):194-202.
Lebrethon M.C., et al. Effects of in vivo and in vitro administration of ghrelin, leptin and neuropeptide mediators on pulsatile gonadotropin-releasing hormone secretion from male rat hypothalamus before and after puberty. J. Neuroendocrinol. 2007, 19(3):181-188.
Lehman M.N., Coolen L.M., Goodman R.L. Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 2010, 151(8):3479-3489.
Leijs M.M., et al. Delayed initiation of breast development in girls with higher prenatal dioxin exposure; a longitudinal cohort study. Chemosphere 2008, 73(6):999-1004.
Leka-Emiri S., et al. Absence of GPR54 and TACR3 mutations in sporadic cases of idiopathic central precocious puberty. Horm. Res. Paediatr. 2014, 81(3):177-181.
Leonhardt M., et al. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol. Reprod. 2003, 68(2):390-400.
Lewis R.W., et al. The effects of the phytoestrogen genistein on the postnatal development of the rat. Toxicol. Sci. 2003, 71(1):74-83.
Li X.F., et al. Role of corticotropin-releasing factor receptor-2 in stress-induced suppression of pulsatile luteinizing hormone secretion in the rat. Endocrinology 2005, 146(1):318-322.
Li X.F., et al. High-fat diet increases LH pulse frequency and kisspeptin-neurokinin B expression in puberty-advanced female rats. Endocrinology 2012, 153(9):4422-4431.
Lie M.E., Overgaard A., Mikkelsen J.D. Effect of a postnatal high-fat diet exposure on puberty onset, estrous cycle regularity, and kisspeptin expression in female rats. Reprod. Biol. 2013, 13(4):298-308.
Lilienthal H., et al. Effects of developmental exposure to 2,2,4,4,5-pentabromodiphenyl ether (PBDE-99) on sex steroids, sexual development, and sexually dimorphic behavior in rats. Environ. Health Perspect. 2006, 114(2):194-201.
Lindgren G. Pubertal stages 1980 of Stockholm schoolchildren. Acta Paediatr. 1996, 85(11):1365-1367.
Lo C.Y., et al. A maternal high-fat diet during pregnancy in rats results in a greater risk of carcinogen-induced mammary tumors in the female offspring than exposure to a high-fat diet in postnatal life. Int. J. Cancer 2009, 125(4):767-773.
Loeffler I.K., Peterson R.E. Interactive effects of TCDD and p, p'-DDE on male reproductive tract development in in utero and lactationally exposed rats. Toxicol. Appl. Pharmacol. 1999, 154(1):28-39.
Lomniczi A., et al. Epigenetic control of female puberty. Nat. Neurosci. 2013, 16(3):281-289.
Losa S.M., et al. Neonatal exposure to genistein adversely impacts the ontogeny of hypothalamic kisspeptin signaling pathways and ovarian development in the peripubertal female rat. Reprod. Toxicol. 2011, 31(3):280-289.
Losa-Ward S.M., et al. Disrupted organization of RFamide pathways in the hypothalamus is associated with advanced puberty in female rats neonatally exposed to bisphenol A. Biol. Reprod. 2012, 87(2):28.
Ma M., et al. Exposure of prepubertal female rats to inhaled di(2-ethylhexyl)phthalate affects the onset of puberty and postpubertal reproductive functions. Toxicol. Sci. 2006, 93(1):164-171.
Ma H.M., et al. Pubertal development timing in urban Chinese boys. Int. J. Androl. 2011, 34(5 Pt 2):e435-e445.
Macedo D.B., et al. Central precocious puberty that appears to be sporadic caused by paternally inherited mutations in the imprinted gene makorin ring finger 3. J. Clin. Endocrinol. Metab. 2014, 99(6):E1097-E1103.
MacLusky N.J., Naftolin F., Leranth C. Immunocytochemical evidence for direct synaptic connections between corticotrophin-releasing factor (CRF) and gonadotrophin-releasing hormone (GnRH)-containing neurons in the preoptic area of the rat. Brain Res. 1988, 439(1-2):391-395.
Maeda K., Ohkura S., Tsukamura H. Physiology of reproduction. The Laboratory Rat 2000, 145-176. Academic Press, London. G.J. Krinke (Ed.).
Maisonet M., et al. Role of prenatal characteristics and early growth on pubertal attainment of British girls. Pediatrics 2010, 126(3):e591-e600.
Maranghi F., et al. Effects of a low oral dose of diethylstilbestrol (DES) on reproductive tract development in F1 female CD-1 mice. Reprod. Toxicol. 2008, 26(2):146-150.
Mieritz M.G., et al. Urinary phthalate excretion in 555 healthy Danish boys with and without pubertal gynaecomastia. Int. J. Androl. 2012, 35(3):227-235.
Moffitt T.E., et al. Childhood experience and the onset of menarche: a test of a sociobiological model. Child Dev. 1992, 63(1):47-58.
Mol N.M., et al. Spermaturia and serum hormone concentrations at the age of puberty in boys prenatally exposed to polychlorinated biphenyls. Eur. J. Endocrinol. 2002, 146(3):357-363.
Monosson E., et al. Peripubertal exposure to the antiandrogenic fungicide, vinclozolin, delays puberty, inhibits the development of androgen-dependent tissues, and alters androgen receptor function in the male rat. Toxicol. Ind. Health 1999, 15(1-2):65-79.
Moral R., et al. The plasticizer butyl benzyl phthalate induces genomic changes in rat mammary gland after neonatal/prepubertal exposure. BMC Genomics 2007, 8:453.
Morrison K.E., et al. Epigenetic mechanisms in pubertal brain maturation. Neuroscience 2013.
Mouritsen A., et al. Urinary phthalates from 168 girls and boys measured twice a year during a 5-year period: associations with adrenal androgen levels and puberty. J. Clin. Endocrinol. Metab. 2013, 98(9):3755-3764.
Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 2008, 28(36):9055-9065.
Mul D., et al. Pubertal development in The Netherlands 1965-1997. Pediatr. Res. 2001, 50(4):479-486.
Murray T.J., et al. Induction of mammary gland ductal hyperplasias and carcinoma in situ following fetal bisphenol A exposure. Reprod. Toxicol. 2007, 23(3):383-390.
Mylchreest E., et al. Dose-dependent alterations in androgen-regulated male reproductive development in rats exposed to Di(n-butyl) phthalate during late gestation. Toxicol. Sci. 2000, 55(1):143-151.
Nagao T., et al. Reproductive function in rats exposed neonatally to bisphenol A and estradiol benzoate. Reprod. Toxicol. 1999, 13:303-311.
Nagao T., et al. Reproductive effects in male and female rats of neonatal exposure to genistein. Reprod. Toxicol. 2001, 15(4):399-411.
Nah W.H., Park M.J., Gye M.C. Effects of early prepubertal exposure to bisphenol A on the onset of puberty, ovarian weights, and estrous cycle in female mice. Clin. Exp. Reprod. Med. 2011, 38(2):75-81.
Navarro V.M., et al. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J. Neurosci. 2012, 32(7):2388-2397.
Nemeroff C.B. New vistas in neuropeptide research in neuropsychiatry: focus on corticotropin-releasing factor. Neuropsychopharmacology 1992, 6(2):69-75.
Nikaido Y., et al. Effects of maternal xenoestrogen exposure on development of the reproductive tract and mammary gland in female CD-1 mouse offspring. Reprod. Toxicol. 2004, 18(6):803-811.
Nikaido Y., et al. Effects of prepubertal exposure to xenoestrogen on development of estrogen target organs in female CD-1 mice. In Vivo 2005, 19(3):487-494.
Niswender K.D., Baskin D.G., Schwartz M.W. Insulin and its evolving partnership with leptin in the hypothalamic control of energy homeostasis. Trends Endocrinol. Metab. 2004, 15(8):362-369.
Noriega N.C., et al. Pubertal administration of DEHP delays puberty, suppresses testosterone production, and inhibits reproductive tract development in male Sprague-Dawley and Long-Evans rats. Toxicol. Sci. 2009, 111(1):163-178.
Odum J., et al. Comparison of the developmental and reproductive toxicity of diethylstilbestrol administered to rats in utero, lactationally, preweaning, or postweaning. Toxicol. Sci. 2002, 68(1):147-163.
Ojeda S.R., Lomniczi A., Sandau U. Contribution of glial-neuronal interactions to the neuroendocrine control of female puberty. Eur. J. Neurosci. 2010, 32(12):2003-2010.
Ojeda S.R., Lomniczi A. Puberty in 2013: unravelling the mystery of puberty. Nat. Rev. Endocrinol. 2014, 10(2):67-69.
Ong K.K., et al. Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J. Clin. Endocrinol. Metab. 2004, 89(6):2647-2651.
Ong K.K., et al. Earlier mother's age at menarche predicts rapid infancy growth and childhood obesity. PLoS Med. 2007, 4(4):e132.
Ong K.K., et al. Genetic variation in LIN28B is associated with the timing of puberty. Nat. Genet. 2009, 41(6):729-733.
Ong K.K., et al. Infancy weight gain predicts childhood body fat and age at menarche in girls. J. Clin. Endocrinol. Metab. 2009, 94(5):1527-1532.
Ong K.K., Ahmed M.L., Dunger D.B. Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol. Cell. Endocrinol. 2006, 254-255:8-12.
Onyango P.O., et al. Puberty and dispersal in a wild primate population. Horm. Behav. 2013, 64(2):240-249.
Ottinger M.A., et al. Establishing appropriate measures for monitoring aging in birds: comparing short and long lived species. Exp. Gerontol. 2003, 38(7):747-750.
Ouyang F., et al. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup. Environ. Med. 2005, 62(12):878-884.
Owen B.M., et al. FGF21 contributes to neuroendocrine control of female reproduction. Nat. Med. 2013, 19(9):1153-1156.
Ozen S., et al. Effects of pesticides used in agriculture on the development of precocious puberty. Environ. Monit. Assess. 2012, 184(7):4223-4232.
Papadimitriou A., et al. Timing of pubertal onset in girls: evidence for non-Gaussian distribution. J. Clin. Endocrinol. Metab. 2008, 93(11):4422-4425.
Parent A.S., et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr. Rev. 2003, 24(5):668-693.
Pascual M., et al. Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rats are associated with ethanol-induced place conditioning. Neuropharmacology 2012, 62(7):2309-2319.
Perry J.R., et al. Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat. Genet. 2009, 41(6):648-650.
Plant T.M. Gonadal regulation of hypothalamic gonadotropin-releasing hormone release in primates. Endocr. Rev. 1986, 7(1):75-88.
Plant T.M. Hypothalamic control of the pituitary-gonadal axis in higher primates: key advances over the last two decades. J. Neuroendocrinol. 2008, 20(6):719-726.
Poling M.C., Kauffman A.S. Organizational and activational effects of sex steroids on kisspeptin neuron development. Front. Neuroendocrinol. 2013, 34(5 Pt 1):3-17.
Politch J.A., Herrenkohl L.R. Effects of prenatal stress on reproduction in male and female mice. Physiol. Behav. 1984, 32(1):95-99.
Polston E.K., Simerly R.B. Ontogeny of the projections from the anteroventral periventricular nucleus of the hypothalamus in the female rat. J. Comp. Neurol. 2006, 495(1):122-132.
Rais-Bahrami K., et al. Follow-up study of adolescents exposed to di(2-ethylhexyl) phthalate (DEHP) as neonates on extracorporeal membrane oxygenation (ECMO) support. Environ. Health Perspect. 2004, 112(13):1339-1340.
Rasier G., et al. Female sexual maturation and reproduction after prepubertal exposure to estrogens and endocrine disrupting chemicals: a review of rodent and human data. Mol. Cell. Endocrinol. 2006, 254-255:187-201.
Rasier G., et al. Early maturation of gonadotropin-releasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol. Reprod. 2007, 77(4):734-742.
Rasier G., et al. Mechanisms of interaction of endocrine-disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone. Toxicol. Sci. 2008, 102(1):33-41.
Rivest S., Plotsky P.M., Rivier C. CRF alters the infundibular LHRH secretory system from the medial preoptic area of female rats: possible involvement of opioid receptors. Neuroendocrinology 1993, 57(2):236-246.
Roa J., Tena-Sempere M. Energy balance and puberty onset: emerging role of central mTOR signaling. Trends Endocrinol. Metab. 2010, 21(9):519-528.
Roelants M., Hauspie R., Hoppenbrouwers K. References for growth and pubertal development from birth to 21years in Flanders, Belgium. Ann. Hum. Biol. 2009, 36(6):680-694.
Rosenfield R.L., Lipton R.B., Drum M.L. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics 2009, 123(1):84-88.
Rothschild T.C., Calhoon R.E., Boylan E.S. Effects of diethylstilbestrol exposure in utero on the genital tracts of female ACI rats. Exp. Mol. Pathol. 1988, 48(1):59-76.
Saillenfait A.M., Sabate J.P., Gallissot F. Diisobutyl phthalate impairs the androgen-dependent reproductive development of the male rat. Reprod. Toxicol. 2008, 26(2):107-115.
Salazar V., et al. Effect of oral intake of dibutyl phthalate on reproductive parameters of Long Evans rats and pre-pubertal development of their offspring. Toxicology 2004, 205(1-2):131-137.
Salvi R., et al. Gonadotropin-releasing hormone expressing neurons immortalized conditionally are activated by insulin: implication of the mitogen-activated protein kinase pathway. Endocrinology 2006, 147(2):816-826.
Sanchez-Garrido M.A., et al. Metabolic programming of puberty: sexually dimorphic responses to early nutritional challenges. Endocrinology 2013, 154(9):3387-3400.
Sanchez-Garrido M.A., Tena-Sempere M. Metabolic control of puberty: roles of leptin and kisspeptins. Horm. Behav. 2013, 64(2):187-194.
Sangiao-Alvarellos S., et al. Changes in hypothalamic expression of the Lin28/let-7 system and related microRNAs during postnatal maturation and after experimental manipulations of puberty. Endocrinology 2013, 154(2):942-955.
Schreiner F., et al. MKRN3 mutations in familial central precocious puberty. Horm. Res. Paediatr. 2014.
Shin J.H., et al. Effects of postnatal administration of diethylstilbestrol on puberty and thyroid function in male rats. J. Reprod. Dev. 2009, 55(5):461-466.
Silveira-Neto A.P., et al. Absence of functional LIN28B mutations in a large cohort of patients with idiopathic central precocious puberty. Horm. Res. Paediatr. 2012, 78(3):144-150.
Sloboda D.M., et al. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 2009, 4(8):e6744.
Sloboda D.M., Hickey M., Hart R. Reproduction in females: the role of the early life environment. Hum. Reprod. Update 2011, 17(2):210-227.
Smith J.T., Spencer S.J. Preweaning over- and underfeeding alters onset of puberty in the rat without affecting kisspeptin. Biol. Reprod. 2012, 86(5):145. 1-8.
Smith J.T., Waddell B.J. Increased fetal glucocorticoid exposure delays puberty onset in postnatal life. Endocrinology 2000, 141(7):2422-2428.
Sorensen K., et al. Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J. Clin. Endocrinol. Metab. 2010, 95(1):263-270.
Stevens A., et al. Pharmacogenomics of insulin-like growth factor-I generation during GH treatment in children with GH deficiency or Turner syndrome. Pharmacogenomics J. 2014, 14(1):54-62.
Stoker T.E., et al. Assessment of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture, in the EDSP male and female pubertal protocols. Toxicol. Sci. 2004, 78(1):144-155.
Strom B.L., et al. Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. J. Am. Med. Assoc. 2001, 286(7):807-814.
Sulem P., et al. Genome-wide association study identifies sequence variants on 6q21 associated with age at menarche. Nat. Genet. 2009, 41(6):734-738.
Suris J.C., Michaud P.A., Viner R. The adolescent with a chronic condition. Part I: Developmental issues. Arch. Dis. Child. 2004, 89(10):938-942.
Tahirovic H.F. Menarchal age and the stress of war: an example from Bosnia. Eur. J. Pediatr. 1998, 157(12):978-980.
Talma H., et al. Trends in menarcheal age between 1955 and 2009 in the Netherlands. PLoS One 2013, 8(4):e60056.
Tan B.L., Kassim N.M., Mohd M.A. Assessment of pubertal development in juvenile male rats after sub-acute exposure to bisphenol A and nonylphenol. Toxicol. Lett. 2003, 143(3):261-270.
Tanner J.M. Growth at Adolescence; with a General Consideration of the Effects of Hereditary and Environmental Factors upon Growth and Maturation from Birth to Maturity 1962, Springfield, Ill., 325 p. second ed.
Teles M.G., et al. A GPR54-activating mutation in a patient with central precocious puberty. N. Engl. J. Med. 2008, 358(7):709-715.
Tena-Sempere M. Ghrelin as a pleotrophic modulator of gonadal function and reproduction. Nat. Clin. Pract. Endocrinol. Metab. 2008, 4(12):666-674.
Terasawa E., Fernandez D.L. Neurobiological mechanisms of the onset of puberty in primates. Endocr. Rev. 2001, 22(1):111-151.
Thamdrup E. Precocious sexual development: a clinical study of one hundred children. Dan. Med. Bull. 1961, 8:140-142.
Tinwell H., et al. Normal sexual development of two strains of rat exposed in utero to low doses of bisphenol A. Toxicol. Sci. 2002, 68(2):339-348.
Tomasiewicz H.C., et al. Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability. Biol. Psychiatry 2012, 72(10):803-810.
Topaloglu A.K., Kotan L.D., Yuksel B. Neurokinin B signalling in human puberty. J. Neuroendocrinol. 2010, 22(7):765-770.
Tsutsui K., et al. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem. Biophys. Res. Commun. 2000, 275:661-667.
Ubuka T., et al. Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J. Comp. Neurol. 2009, 517:841-855.
Urban R.J., et al. Acute androgen receptor blockade increases luteinizing hormone secretory activity in men. J. Clin. Endocrinol. Metab. 1988, 67(6):1149-1155.
van Noord P.A., Kaaks R. The effect of wartime conditions and the 1944-45 'Dutch famine' on recalled menarcheal age in participants of the DOM breast cancer screening project. Ann. Hum. Biol. 1991, 18(1):57-70.
Vasiliu O., Muttineni J., Karmaus W. In utero exposure to organochlorines and age at menarche. Hum. Reprod. 2004, 19(7):1506-1512.
Vercauteren M., Susanne C. The secular trend of height and menarche in Belgium: are there any signs of a future stop?. Eur. J. Pediatr. 1985, 144(4):306-309.
Vulliémoz N.R., et al. Decrease in luteinizing hormone pulse frequency during a five-hour peripheral ghrelin infusion in the ovariectomized rhesus monkey. J. Clin. Endocrinol. Metab. 2004, 89(11):5718-5723.
Warner M., et al. Serum dioxin concentrations and age at menarche. Environ. Health Perspect. 2004, 112(13):1289-1292.
Warren M.P., Fried J.L. Hypothalamic amenorrhea. The effects of environmental stresses on the reproductive system: a central effect of the central nervous system. Endocrinol. Metab. Clin. North Am. 2001, 30(3):611-629.
Wehkalampi K., et al. Genetic and environmental influences on pubertal timing assessed by height growth. Am. J. Hum. Biol. 2008, 20(4):417-423.
Wierson M., Long P.J., Forehand R.L. Toward a new understanding of early menarche: the role of environmental stress I pubertal timing. Adolescence 1993, 28(112):913-924.
Willoughby K.N., et al. Neonatally administered tert-octylphenol affects onset of puberty and reproductive development in female rats. Endocrine 2005, 26(2):161-168.
Wolfe A., Divall S., Wu S. The regulation of reproductive neuroendocrine function by insulin and insulin-like growth factor-1 (IGF-1). Front. Neuroendocrinol. 2014, 35(4):558-572.
Wolff M.S., et al. Environmental exposures and puberty in inner-city girls. Environ. Res. 2008, 107(3):393-400.
Worley G., et al. Secondary sexual characteristics in children with cerebral palsy and moderate to severe motor impairment: a cross-sectional survey. Pediatrics 2002, 110(5):897-902.
Wu S., et al. Dynamic epigenetic changes involved in testicular toxicity induced by di-2-(ethylhexyl)phthalate in mice. Basic Clin. Pharmacol. Toxicol. 2010, 106(2):118-123.
Yamamoto M., et al. Effects of maternal exposure to diethylstilbestrol on the development of the reproductive system and thyroid function in male and female rat offspring. J. Toxicol. Sci. 2003, 28(5):385-394.
Yang C.Y., et al. The endocrine and reproductive function of the female Yucheng adolescents prenatally exposed to PCBs/PCDFs. Chemosphere 2005, 61(3):355-360.
Yoshimura S., et al. Observation of preputial separation is a useful tool for evaluating endocrine active chemicals. J. Toxicol. Pathol. 2005, 18:141-157.
Yu B., et al. Estrogen receptor alpha and beta expressions in hypothalamus-pituitary-ovary axis in rats exposed lactationally to soy isoflavones and bisphenol A. Biomed. Environ. Sci. 2010, 23(5):357-362.
Zachmann M., et al. Pubertal growth in patients with androgen insensitivity: indirect evidence for the importance of estrogens in pubertal growth of girls. J. Pediatr. 1986, 108(5 Pt 1):694-697.
Zhang Y., et al. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372(6505):425-432.