Background
Given the established relation between testosterone and aging in older adults, we
tested whether buccal telomere length (TL), an established cellular biomarker of aging,
was associated with testosterone levels in youth.
Methods
Children, mean age 10.2 years, were recruited from the greater New orleans area, and salivary testosterone
was measured diurnally and during an acute stressor. Buccal TL was measured using
monochrome multiplex quantitative real-time polymerase chain reaction. Testosterone
and TL data were available on 77 individuals. The association between buccal TL and
testosterone was tested using multivariate generalized estimating equations to account
for clustering of children within families.
Results
Greater peak testosterone levels (β=−0.87, P<0.01) and slower recovery (β=−0.56, P<0.01) and reactivity (β=–1.22, P<0.01) following a social stressor were significantly associated with shorter buccal
TL after controlling for parental age at conception, child age, sex, sociodemographic
factors and puberty. No association was initially present between diurnal measurements
of testosterone or morning basal testosterone levels and buccal TL. Sex significantly
moderated the relation between testosterone reactivity and buccal TL.
Conclusions
The association between testosterone and buccal TL supports gonadal maturation as
a developmentally sensitive biomarker of aging within youth. As stress levels of testosterone
were significantly associated with buccal TL, these findings are consistent with the
growing literature linking stress exposure and accelerated maturation. The lack of
association of diurnal testosterone or morning basal levels with buccal TL bolsters
the notion of a shared stress-related maturational mechanism between cellular stress
and the hypothalamic pituitary gonadal axis. These data provide novel evidence supporting
the interaction of aging, physiologic stress and cellular processes as an underlying
mechanism linking negative health outcomes and early life stress.
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REFERENCES
- Stress and telomere biology: a lifespan perspective.Psychoneuroendocrinology. 2013;
- Neighborhood disorder and telomeres: Connecting children’s exposure to community level stress and cellular response.Soc Sci Med. 2013; 85: 50-58
- Cell aging in relation to stress arousal and cardiovascular disease risk factors.Psychoneuroendocrinology. 2006; 31: 277-287
- Telomeres and type 2 diabetes.Transl Res. 2010; 155: 164-165
- Exogenous application of glucose induces aging in rat cerebral oligodendrocytes as revealed by alteration in telomere length.Neurosci Lett. 2004; 368: 68-72
- Factors that influence telomeric oxidative base damage and repair by DNA glycosylase OGG1.DNA Repair (Amst). 2011; 10: 34-44
- Telomere length and early severe social deprivation: linking early adversity and cellular aging.Mol Psychiatry. 2012; 17: 719-727
- Exposure to violence during childhood is associated with telomere erosion from 5 to 10 years of age: a longitudinal study.Mol Psychiatry. 2013; 18: 576-581
- Socioeconomic status and cell aging in children.Soc Sci Med. 2012; 74: 1948-1951
- The “trouble” with salivary testosterone.Psychoneuroendocrinology. 2004; 29: 1229-1240
- Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents.Dev Cogn Neurosci. 2011; 1: 506-516
- Sex steroids and the organization of the human brain.J Neurosci. 2012; 32: 6745-6746
- A single administration of testosterone reduces fearpotentiated startle in humans.Biol Psychiatry. 2006; 59: 872-874
- Basal testosterone moderates responses to anger faces in humans.Physiol Behav. 2007; 90: 496-505
- Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women.Neuroimage. 2010; 52: 277-283
- Are salivary gonadal steroid concentrations influenced by acutepsychosocial stress? A study using the Trier Social Stress Test (TSST).Int J Psychophysiol. 2011; 80: 36-43
- Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis.Psychosom Medicine. 1997; 59: 419-426
- Correlations among salivary testosterone, mood, and selective attention to threat in humans.Horm Behav. 1999; 36: 17-24
- Pubertal development: correspondence between hormonal and physical development.Child Dev. 2009; 80: 327-337
- Salivary testosterone diurnal variation and psychopathology in adolescent males and females: individual differences and developmental effects.Dev Psychopathol. 2003; 15: 431-449
- Diurnal and seasonal cortisol, testosterone, and DHEA rhythms in boys and girls during puberty.Chronobiol Int. 2007; 24: 969-990
- Are adolescents the victims of raging hormones: evidence for activational effects of hormones on moods and behavior at adolescence.Psychol Bull. 1992; 111: 62-107
- Testosterone in newly diagnosed, antipsychoticnaive men with nonaffective psychosis: a test of the accelerated aging hypothesis.Psychosom Med. 2011; 73: 643-647
- Defining the boundaries of early adolescence: a user’s guide to assessing pubertal status and pubertal timing in research with adolescents.Appl Developmental Sci. 2006; 10: 30-56
- The neural basis of puberty and adolescence.Nat Neurosci. 2004; 7: 1040-1047
- Androgens, brain, and behavior.Am J Psychiatry. 1996; 153: 974-984
- Androgens and puberty.Best Pract Res Clin Endocrinol Metab. 2002; 16: 31-41
- Self-assessment of physical sexual maturation in boys and girls with delayed puberty.J Adolesc Health. 1999; 25: 379-381
- Diversity of pubertal testosterone changes in boys with constitutional delay in growth and/or adolescence.J Pediatr Endocrinol Metab. 1997; 10: 395-400
- Gender differences in testosterone and cortisol response to competition.Psychoneuroendocrinology. 2005; 30: 58-71
- Testosterone and men’s health.J Behav Med. 1999; 22: 1-19
- Telomerase activity in the testis of infertile patients with selected causes.Hum Reprod. 1998; 13: 1476-1479
- Telomerase is activated in the prostate and seminal vesicles of the castrated rat.Endocrinology. 1996; 137: 5743-5746
- Free radical theory of aging: implications in male infertility.Urology. 2010; 75: 14-19
- Aging gonads, glands, and gametes: immutable or partially reversible changes?.Fertil Steril. 2013; 99: 1-4
- Telomere length versus hormonal and bone mineral status in healthy elderly men.Mech Ageing Dev. 2005; 126: 1115-1122
- Telomere length measurement by a novel monochrome multiplex quantitative PCR method.Nucleic Acids Res. 2009; 37: e21
- Paternal age at birth is associated with offspring leukocyte telomere length in the Nurses’ Health Study.Hum Reprod. 2012; 29: 3622-3631
- A self-report measure of pubertal status: Reliability, validity, and initial norms.J Youth Adolesc. 1988; 17: 117-133
- Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context.Dev Psychopathol. 2011; 23: 85-99
- Paternal age at birth is an important determinant of offspring telomere length.Hum Mol Genet. 2007; 16: 3097-3102
- Timing of pubertal maturation in girls: an integrated life history approach.Psychol Bull. 2004; 130: 920-958
- It’s about timing and change: pubertal transition effects on symptoms of major depression among African American youths.Dev Psychol. 2003; 39: 430-439
- The role of immaturity in human development.Psychol Bull. 1997; 122: 153-169
- The adaptive calibration model of stress responsivity.Neurosci Biobehav Rev. 2011; 35: 1562-1592
- Childhood experience, interpersonal development, and reproductive srategy: an evolutionary theory of socialization.Child Dev. 1991; 62: 642-670
- A life-history model of human fitness indicators.Biodemography Soc Biol. 2010; 56: 42-66
- The behavioral correlates of overall and distinctive life history strategy.J Pers Soc Psychol. 2013; 105: 873-888
- The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the tradeoffs in health and disease.Neurosci Biobehav Rev. 2005; 29: 3-38
- The concept of allostasis in biology and biomedicine.Horm Behav. 2003; 43: 2-15
- Family environments, adrenarche, and sexual maturation: a longitudinal test of a life history model.Child Dev. 2007; 78: 1799-1817
- Beyond the stress concept: allostatic Load—a developmental biological and cognitive perspective.in: Cicchetti D. Cohen D. Developmental Psychopathology. 2nd ed. John Wiley & Sons, Hoboken, NJ2006: 578-628
- Neighborhood disorder and telomeres: Connecting children’s exposure to community level stress and cellular response.Soc Sci Med. 2013; 85: 50-58
- Potential biomarkers of ageing.Biol Chem. 2008; 389: 257-265
- Salivary dehydroepiandrosterone responsiveness to social challenge in adolescents with internalizing problems.J Child Psychol Psychiatry. 2007; 48: 580-591
- Testosterone cannot activate an adult-like stress response in prepubertal male rats.Neuroendocrinology. 2004; 79: 125-132
- Hormonal reactivity to MRI scanning in adolescents.Psychoneuroendocrinology. 2009; 34: 1242-1246
- Psychopathy’s influence on the coupling between hypothalamic-pituitary-adrenal and -gonadal axes among incarcerated adolescents.Developmental Psychobiology. 2013; 56: 448-458
- Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress.Dev Psychobiol. 2013
- Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus.Gen Comp Endocrinol. 1991; 81: 217-226
- Individual differences in boys’ and girls’ timing and tempo of puberty: modeling development with nonlinear growth models.Dev Psychol. 2011; 47: 1389-1409
- Serum androgen bioactivity in adolescence: a longitudinal study of boys with constitutional delay of puberty.J Clin Endocrinol Metab. 2004; 89: 1188-1192
- Race, race-based discrimination, and health outcomes among African Americans.Annu Rev Psychol. 2007; 58: 201-225
- Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies.Epigenetics. 2013; 8: 1-10
Article info
Footnotes
Supported by the National Institutes of Health (1R01ES020447-01 to K.P.T., R21 MH094688-01 to S.S.D.) and Tulane University Oliver Scholars Fund (S.S. D.). The project described was also supported by Award Number K12HD043451 (to S.S.D.) from the Eunice Kennedy Shriver National Institute of Child Health & Human Development. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Eunice Kennedy Shriver National Institute of Child Health & Human Development or the National Institutes of Health.
The authors have no conflicts of interest to disclose.
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© 2014 Southern Society for Clinical Investigation. Published by Elsevier Inc. All rights reserved.
