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Aging, glucocorticoids and developmental programming

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Abstract

Glucocorticoids are pleiotropic regulators of multiple cell types with critical roles in physiological systems that change across the life-course. Although glucocorticoids have been associated with aging, available data on the aging trajectory in basal circulating glucocorticoids are conflicting. A literature search reveals sparse life-course data. We evaluated (1) the profile of basal circulating corticosterone across the life-course from weaning (postnatal day—PND 21), young adult PND 110, adult PND 450, mature adult PND 650 to aged phase PND 850 in a well-characterized homogeneous rat colony to determine existence of significant changes in trajectory in the second half of life; (2) sex differences; and (3) whether developmental programming of offspring by exposure to maternal obesity during development alters the later-life circulating corticosterone trajectory. We identified (1) a fall in corticosterone between PND 450 and 650 in both males and females (p < 0.05) and (2) higher female than male concentrations (p < 0.05). (3) Using our five life-course time-point data set, corticosterone fell at a similar age but from higher levels in male and female offspring of obese mothers. In all four groups studied, there was a second half of life fall in corticosterone. Higher corticosterone levels in offspring of obese mothers may play a role in their shorter life-span, but the age-associated fall occurs at a similar time to control offspring. Although even more life-course time-points would be useful, a five life-course time-point analysis provides important new information on normative and programmed aging of circulating corticosterone.

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Abbreviations

BMI:

Body mass index

C:

Control

dG:

Days gestation

PND:

Postnatal day

References

  • Anderson RM, Birnie AK, Koblesky NK, Romig-Martin SA, Radley JJ (2014) Adrenocortical status predicts the degree of age-related deficits in prefrontal structural plasticity and working memory. J Neurosci 34:8387–8397. doi:10.1523/JNEUROSCI.1385-14.2014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bergendahl M, Iranmanesh A, Mulligan T, Veldhuis JD (2000) Impact of age on cortisol secretory dynamics basally and as driven by nutrient-withdrawal stress. J Clin Endocrinol Metab 85:2203–2214. doi:10.1210/jcem.85.6.6628

    CAS  PubMed  Google Scholar 

  • Bowman RE, Maclusky NJ, Diaz SE, Zrull MC, Luine VN (2006) Aged rats: sex differences and responses to chronic stress. Brain Res 1126:156–166. doi:10.1016/j.brainres.2006.07.047

    Article  CAS  PubMed  Google Scholar 

  • Braun T, Challis JR, Newnham JP, Sloboda DM (2013) Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr Rev 34:885–916. doi:10.1210/er.2013-1012

    Article  CAS  PubMed  Google Scholar 

  • Chen KC et al (2013) Glucocorticoid-dependent hippocampal transcriptome in male rats: pathway-specific alterations with aging. Endocrinology 154:2807–2820. doi:10.1210/en.2013-1139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Downs JL, Mattison JA, Ingram DK, Urbanski HF (2008) Effect of age and caloric restriction on circadian adrenal steroid rhythms in rhesus macaques. Neurobiol Aging 29:1412–1422. doi:10.1016/j.neurobiolaging.2007.03.011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ferrari E et al (2001) Age-related changes of the hypothalamic-pituitary-adrenal axis: pathophysiological correlates. Eur J Endocrinol 144:319–329

    Article  CAS  PubMed  Google Scholar 

  • Guo C, Li C, Myatt L, Nathanielsz PW, Sun K (2013) Sexually dimorphic effects of maternal nutrient reduction on expression of genes regulating cortisol metabolism in fetal baboon adipose and liver tissues. Diabetes 62:1175–1185. doi:10.2337/db12-0561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang CW, Lui CC, Chang WN, Lu CH, Wang YL, Chang CC (2009) Elevated basal cortisol level predicts lower hippocampal volume and cognitive decline in Alzheimer’s disease. J Clin Neurosci 16:1283–1286. doi:10.1016/j.jocn.2008.12.026

    Article  CAS  PubMed  Google Scholar 

  • Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J (2010) Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5, e10074. doi:10.1371/journal.pone.0010074

    Article  PubMed Central  PubMed  Google Scholar 

  • Kral JG, Biron S, Simard S, Hould FS, Lebel S, Marceau S, Marceau P (2006) Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 118:e1644–e1649. doi:10.1542/peds.2006-1379

    Article  PubMed  Google Scholar 

  • Langie SA, Lara J, Mathers JC (2012) Early determinants of the ageing trajectory. Best Pract Res Clin Endocrinol Metab 26:613–626. doi:10.1016/j.beem.2012.03.004

    Article  CAS  PubMed  Google Scholar 

  • Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother-infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol Behav 96:613–619. doi:10.1016/j.physbeh.2008.12.016

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nathanielsz PW, Ford SP, Long NM, Vega CC, Reyes-Castro LA, Zambrano E (2013) Interventions to prevent adverse fetal programming due to maternal obesity during pregnancy. Nutr Rev 71(Suppl 1):S78–S87. doi:10.1111/nure.12062

    Article  PubMed Central  PubMed  Google Scholar 

  • National Research Council (2011) Explaining divergent levels of longevity in high-income countries. In: Crimmins EM, Preston SH, Cohen B (eds) Panel on understanding divergent trends in longevity in high-income countries. Committee on population, division of behavioral and social sciences and education. The National Academies Press, Washington DC

    Google Scholar 

  • Nivoit P, Morens C, Van Assche FA, Jansen E, Poston L, Remacle C, Reusens B (2009) Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia 52:1133–1142. doi:10.1007/s00125-009-1316-9

    Article  CAS  PubMed  Google Scholar 

  • Peeters GM, van Schoor NM, Visser M, Knol DL, Eekhoff EM, de Ronde W, Lips P (2007) Relationship between cortisol and physical performance in older persons. Clin Endocrinol 67:398–406. doi:10.1111/j.1365-2265.2007.02900.x

    Article  CAS  Google Scholar 

  • Quinn R (2005) Comparing rat’s to human’s age: how old is my rat in people years? Nutrition 21:775–777. doi:10.1016/j.nut.2005.04.002

    Article  PubMed  Google Scholar 

  • Rodriguez JS et al (2012) Maternal obesity in the rat programs male offspring exploratory, learning and motivation behavior: prevention by dietary intervention pre-gestation or in gestation. Int J Dev Neurosci 30:75–81. doi:10.1016/j.ijdevneu.2011.12.012

    Article  CAS  PubMed  Google Scholar 

  • Samuelsson AM et al (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51:383–392. doi:10.1161/HYPERTENSIONAHA.107.101477

    Article  CAS  PubMed  Google Scholar 

  • Vega CC, Reyes-Castro LA, Bautista CJ, Larrea F, Nathanielsz PW, Zambrano E (2015) Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes (Lond) 39(4):712–719. doi:10.1038/ijo.2013.150

  • Villamor E, Cnattingius S (2006) Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study. Lancet 368:1164–1170. doi:10.1016/S0140-6736(06)69473-7

    Article  PubMed  Google Scholar 

  • Zambrano E, Nathanielsz PW (2013) Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutr Rev 71(Suppl 1):S42–S54. doi:10.1111/nure.12068

    Article  PubMed  Google Scholar 

  • Zambrano E, Martinez-Samayoa PM, Rodriguez-Gonzalez GL, Nathanielsz PW (2010) Dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats. J Physiol 588:1791–1799. doi:10.1113/jphysiol.2010.190033

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zambrano E et al (2014) Increased central and peripheral glucocorticoid synthesis act as an orchestrator of developmental programming. In: stress and developmental programming of health and disease: beyond phenomenology nova Science Publishers, Inc

  • Zhao ZY, Lu FH, Xie Y, Fu YR, Bogdan A, Touitou Y (2003) Cortisol secretion in the elderly. Influence of age, sex and cardiovascular disease in a Chinese population. Steroids 68:551–555

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

LARC is a graduate student from Doctorado en Ciencias Biomédicas, Facultad de Medicina, Universidad Nacional Autónoma de México and is a recipient of the CONACyT fellowship; this work was supported by CONACyT 155166 México. We are grateful to Guadalupe L. Rodríguez-González for assistance with the manuscript.

Conflict of interest

The authors have nothing to disclose and have no conflict of interest.

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Authors and Affiliations

  1. Reproductive Biology Department, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, 14000, Mexico

    E. Zambrano & L. A. Reyes-Castro

  2. Department of Animal Science, University of Wyoming, Laramie, WY, 82071-3684, USA

    P. W. Nathanielsz

Authors
  1. E. Zambrano
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  2. L. A. Reyes-Castro
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  3. P. W. Nathanielsz
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Correspondence to P. W. Nathanielsz.

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Zambrano, E., Reyes-Castro, L.A. & Nathanielsz, P.W. Aging, glucocorticoids and developmental programming. AGE 37, 52 (2015). https://doi.org/10.1007/s11357-015-9774-0

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