Long-term multi-organ system abnormalities in mice exposed to antenatal and postnatal corticosteroids

Long-term multi-organ system abnormalities in mice exposed to antenatal and postnatal corticosteroids
  • Crump, C. An overview of adult health outcomes after preterm birth. Early Hum. Dev. 150, 105187, (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lurbe, E. & Ingelfinger, J. Developmental and early life origins of cardiometabolic risk factors: novel findings and implications. Hypertension 77, 308–318, (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Rog-Zielinska, E. A., Richardson, R. V., Denvir, M. A. & Chapman, K. E. Glucocorticoids and foetal heart maturation; implications for prematurity and foetal programming. J. Mol. Endocrinol. 52, R125–R135, (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Asztalos, E. Antenatal corticosteroids: a risk factor for the development of chronic disease. J. Nutr. Metab. 2012, 930591, (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Busada, J. T. & Cidlowski, J. A. Mechanisms of glucocorticoid action during development. Curr. Top. Dev. Biol. 125, 147–170, (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Braun, T., Challis, J. R., Newnham, J. P. & Sloboda, D. M. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr. Rev. 34, 885–916, (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Committee on Obstetric, P Committee opinion No. 713: antenatal corticosteroid therapy for fetal maturation. Obstet. Gynecol. 130, e102–e109, (2017).

    Article 
    CAS 

    Google Scholar 

  • Kemp, M. W. et al. Efficacy and safety of antenatal steroids. Am. J. Physiol. Regul. Integr. Comp. Physiol. 315, R825–R839, (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Roberts, D., Brown, J., Medley, N. & Dalziel, S. R. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst. Rev. 3, CD004454, (2017).

    Article 
    PubMed 

    Google Scholar 

  • Doyle, L. W., Cheong, J. L., Hay, S., Manley, B. J. & Halliday, H. L. Late (>/= 7 days) systemic postnatal corticosteroids for prevention of bronchopulmonary dysplasia in preterm infants. Cochrane Database Syst. Rev. 11, CD001145, (2021).

    Article 
    PubMed 

    Google Scholar 

  • Lok, I. M. et al. Effects of postnatal corticosteroids on lung development in newborn animals. A systematic review. Pediatr. Res. (2024).

  • Harris, C. et al. Postnatal dexamethasone exposure and lung function in adolescents born very prematurely. PLoS One 15, e0237080, (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vrselja, A., Pillow, J. J. & Black, M. J. Effect of preterm birth on cardiac and cardiomyocyte growth and the consequences of antenatal and postnatal glucocorticoid treatment. J. Clin. Med. 10 (2021).

  • Festing, M. F. & Altman, D. G. Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J. 43, 244–258, (2002).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Li, H., Yuan, X., Tang, J. & Zhang, Y. Lipopolysaccharide disrupts the directional persistence of alveolar myofibroblast migration through EGF receptor. Am. J. Physiol. Lung Cell Mol. Physiol. 302, L569–L579, (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cooney, T. P. & Thurlbeck, W. M. The radial alveolar count method of Emery and Mithal: a reappraisal 1–postnatal lung growth. Thorax 37, 572–579, (1982).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Emery, J. L. & Mithal, A. The number of alveoli in the terminal respiratory unit of man during late intrauterine life and childhood. Arch. Dis. Child 35, 544–547, (1960).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Xu, J. et al. GDF15/MIC-1 functions as a protective and antihypertrophic factor released from the myocardium in association with SMAD protein activation. Circ. Res. 98, 342–350, (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wallner, M. et al. Acute catecholamine exposure causes reversible myocyte injury without cardiac regeneration. Circ. Res 119, 865–879, (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hillman, N. H. et al. Dose of budesonide with surfactant affects lung and systemic inflammation after normal and injurious ventilation in preterm lambs. Pediatr. Res. 88, 726–732, (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cummings, J. J., Pramanik, A. K., Committee On, F. & Newborn. Postnatal corticosteroids to prevent or treat chronic lung disease following preterm birth. Pediatrics 149 (2022).

  • Jobe, A. H., Milad, M. A., Peppard, T. & Jusko, W. J. Pharmacokinetics and pharmacodynamics of intramuscular and oral betamethasone and dexamethasone in reproductive age women in India. Clin. Transl. Sci. 13, 391–399, (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tijsseling, D. et al. Neonatal corticosteroid therapy affects growth patterns in early infancy. PLoS One 13, e0192162, (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Regan, F. M., Cutfield, W. S., Jefferies, C., Robinson, E. & Hofman, P. L. The impact of early nutrition in premature infants on later childhood insulin sensitivity and growth. Pediatrics 118, 1943–1949, (2006).

    Article 
    PubMed 

    Google Scholar 

  • Singhal, A. Early nutrition and long-term cardiovascular health. Nutr. Rev. 64, S44–S49, (2006). discussion S72-91.

    Article 
    PubMed 

    Google Scholar 

  • Singhal, A., Cole, T. J., Fewtrell, M., Deanfield, J. & Lucas, A. Is slower early growth beneficial for long-term cardiovascular health? Circulation 109, 1108–1113, (2004).

    Article 
    PubMed 

    Google Scholar 

  • Qin, G. et al. Postnatal dexamethasone, respiratory and neurodevelopmental outcomes at two years in babies born extremely preterm. PLoS One 12, e0181176, (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Harris, C. et al. Effect of dexamethasone exposure on the neonatal unit on the school age lung function of children born very prematurely. PLoS One 13, e0200243, (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Evans, N. Cardiovascular effects of dexamethasone in the preterm infant. Arch. Dis. Child Fetal Neonatal Ed. 70, F25–F30, (1994).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gill, A. W., Warner, G. & Bull, L. Iatrogenic neonatal hypertrophic cardiomyopathy. Pediatr. Cardiol. 17, 335–339, (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Werner, J. C. et al. Hypertrophic cardiomyopathy associated with dexamethasone therapy for bronchopulmonary dysplasia. J. Pediatr. 120, 286–291, (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zecca, E. et al. Cardiac adverse effects of early dexamethasone treatment in preterm infants: a randomized clinical trial. J. Clin. Pharm. 41, 1075–1081, (2001).

    Article 
    CAS 

    Google Scholar 

  • Skelton, R., Gill, A. B. & Parsons, J. M. Cardiac effects of short course dexamethasone in preterm infants. Arch. Dis. Child Fetal Neonatal Ed. 78, F133–F137, (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ohning, B. L., Fyfe, D. A. & Riedel, P. A. Reversible obstructive hypertrophic cardiomyopathy after dexamethasone therapy for bronchopulmonary dysplasia. Am. Heart J. 125, 253–256, (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • de Vries, W. B. et al. Alterations in adult rat heart after neonatal dexamethasone therapy. Pediatr. Res 52, 900–906, (2002).

    Article 
    PubMed 

    Google Scholar 

  • Bal, M. P. et al. Histopathological changes of the heart after neonatal dexamethasone treatment: studies in 4-, 8-, and 50-week-old rats. Pediatr. Res 66, 74–79, (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Niu, Y., Herrera, E. A., Evans, R. D. & Giussani, D. A. Antioxidant treatment improves neonatal survival and prevents impaired cardiac function at adulthood following neonatal glucocorticoid therapy. J. Physiol. 591, 5083–5093, (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bal, M. P. et al. Long-term cardiovascular effects of neonatal dexamethasone treatment: hemodynamic follow-up by left ventricular pressure-volume loops in rats. J. Appl Physiol. (1985) 104, 446–450, (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kamphuis, P. J. et al. Reduced life expectancy in rats after neonatal dexamethasone treatment. Pediatr. Res 61, 72–76, (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Jiang, X. et al. Effects of neonatal dexamethasone administration on cardiac recovery ability under ischemia-reperfusion in 24-wk-old rats. Pediatr. Res. 80, 128–135, (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Cardoso, R. C. & Padmanabhan, V. Prenatal steroids and metabolic dysfunction: lessons from sheep. Annu. Rev. Anim. Biosci. 7, 337–360, (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Fowden, A. L., Giussani, D. A. & Forhead, A. J. Intrauterine programming of physiological systems: causes and consequences. Physiology (Bethesda) 21, 29–37, (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Jellyman, J. K., Valenzuela, O. A. & Fowden, A. L. HORSE SPECIES SYMPOSIUM: glucocorticoid programming of hypothalamic-pituitary-adrenal axis and metabolic function: Animal studies from mouse to horse. J. Anim. Sci. 93, 3245–3260, (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Leone, T. C. et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101, (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Besse-Patin, A. et al. Estrogen signals through peroxisome proliferator-activated receptor-gamma coactivator 1alpha to reduce oxidative damage associated with diet-induced fatty liver disease. Gastroenterology 152, 243–256, (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Estall, J. L. et al. Sensitivity of lipid metabolism and insulin signaling to genetic alterations in hepatic peroxisome proliferator-activated receptor-gamma coactivator-1alpha expression. Diabetes 58, 1499–1508, (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kleiner, S. et al. Development of insulin resistance in mice lacking PGC-1alpha in adipose tissues. Proc. Natl. Acad. Sci. USA 109, 9635–9640, (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lopez-Otin, C., Blasco, M. A., Partridge, L., Serrano, M. & Kroemer, G. The hallmarks of aging. Cell 153, 1194–1217, (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, Y. et al. Mitochondrial aldehyde dehydrogenase 2 accentuates aging-induced cardiac remodeling and contractile dysfunction: role of AMPK, Sirt1, and mitochondrial function. Free Radic. Biol. Med. 71, 208–220, (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lemieux, H., Vazquez, E. J., Fujioka, H. & Hoppel, C. L. Decrease in mitochondrial function in rat cardiac permeabilized fibers correlates with the aging phenotype. J. Gerontol. A Biol. Sci. Med. Sci. 65, 1157–1164, (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Owesny, P. & Grune, T. The link between obesity and aging – insights into cardiac energy metabolism. Mech. Ageing Dev. 216, 111870. (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Balsan, G. A., Vieira, J. L., Oliveira, A. M. & Portal, V. L. Relationship between adiponectin, obesity and insulin resistance. Rev. Assoc. Med. Bras. (1992) 61, 72–80, (2015).

    Article 
    PubMed 

    Google Scholar 

  • Jung, U. J. & Choi, M. S. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int. J. Mol. Sci. 15, 6184–6223, (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hulthe, J., Hulten, L. M. & Fagerberg, B. Low adipocyte-derived plasma protein adiponectin concentrations are associated with the metabolic syndrome and small dense low-density lipoprotein particles: atherosclerosis and insulin resistance study. Metabolism 52, 1612–1614, (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Crume, T. L. et al. The long-term impact of intrauterine growth restriction in a diverse U.S. cohort of children: the EPOCH study. Obesity (Silver Spring) 22, 608–615, (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ordonez-Diaz, M. D. et al. Plasma adipokines profile in prepubertal children with a history of prematurity or extrauterine growth restriction. Nutrients 12 (2020).

  • Dai, Y. et al. Prenatal prednisone exposure impacts liver development and function in fetal mice and its characteristics. Toxicol. Sci. 199, 63–80, (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Nair, A. B. & Jacob, S. A simple practice guide for dose conversion between animals and human. J. Basic Clin. Pharm. 7, 27–31, (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schittny, J. C. Development of the lung. Cell Tissue Res. 367, 427–444, (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nguyen, T. & Jordan, B. K. Let’s talk about dex: when do the benefits of dexamethasone for prevention of bronchopulmonary dysplasia outweigh the risks?. Newborn (Clarksville) 1, 91–96, (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dutta, S. & Sengupta, P. Men and mice: relating their ages. Life Sci. 152, 244–248, (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Effect of corticosteroids for fetal maturation on perinatal outcomes NIH consensus development panel on the effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA 273, 413–418, (1995).

    Article 

    Google Scholar 

  • Kim, Y. E., Park, W. S., Sung, D. K., Ahn, S. Y. & Chang, Y. S. Antenatal betamethasone enhanced the detrimental effects of postnatal dexamethasone on hyperoxic lung and brain injuries in newborn rats. PLoS One 14, e0221847, (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ersek, A. et al. Strain dependent differences in glucocorticoid-induced bone loss between C57BL/6J and CD-1 mice. Sci. Rep. 6, 36513. (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hodes, G. E. et al. Strain differences in the effects of chronic corticosterone exposure in the hippocampus. Neuroscience 222, 269–280, (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Shelton, E. L. et al. Effects of antenatal betamethasone on preterm human and mouse ductus arteriosus: comparison with baboon data. Pediatr. Res. 84, 458–465, (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, H. et al. The angiogenic factor midkine is regulated by dexamethasone and retinoic acid during alveolarization and in alveolar epithelial cells. Respir. Res. 10, 77, (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Krishnan, A. et al. A detailed comparison of mouse and human cardiac development. Pediatr. Res. 76, 500–507, (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wessels, A. & Sedmera, D. Developmental anatomy of the heart: a tale of mice and man. Physiol. Genom. 15, 165–176, (2003).

    Article 

    Google Scholar 

  • Kaffe, E. et al. Humanized mouse liver reveals endothelial control of essential hepatic metabolic functions. Cell 186, 3793–3809 e3726, (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vickers, M. H. Developmental programming and transgenerational transmission of obesity. Ann. Nutr. Metab. 64, 26–34, (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Buescher, J. L. et al. Evidence for transgenerational metabolic programming in Drosophila. Dis. Model Mech. 6, 1123–1132, (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, Z., Cao, F. & Li, X. Epigenetic programming and fetal metabolic programming. Front Endocrinol. (Lausanne) 10, 764, (2019).

    Article 
    PubMed 

    Google Scholar 

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