Excess of glucocorticoids during late gestation impairs the recovery of offspring's β-cell function after a postnatal injury.

Szczegóły
Abstrakt

Tytuł:: Excess of glucocorticoids during late gestation impairs the recovery of offspring's β-cell function after a postnatal injury.
Autorzy:: Dos Santos C; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Rafacho A; Laboratory of Investigation in Chronic Diseases - LIDoC, Department of Physiological Sciences, Center of Biological Sciences, Federal University of Santa Catarina - UFSC, Florianópolis, Brazil.
Ferreira SM; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Vettorazzi JF; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Dos Reis Araújo T; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Mateus Gonçalves L; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Ruhrmann S; Epigenetics and Diabetes Unit, Department of Clinical Sciences Malmö, Lund University Diabetes Center, Scania University Hospital, Malmö, Sweden.
Bacos K; Epigenetics and Diabetes Unit, Department of Clinical Sciences Malmö, Lund University Diabetes Center, Scania University Hospital, Malmö, Sweden.
Ling C; Epigenetics and Diabetes Unit, Department of Clinical Sciences Malmö, Lund University Diabetes Center, Scania University Hospital, Malmö, Sweden.
Boschero AC; Laboratory of Endocrine Pancreas and Metabolism - LAPEM, Department of Structural and Functional Biology, Institute of Biology, Campinas State University - UNICAMP, Campinas, Brazil.
Jorge Dos Santos G; Laboratory of Investigation in Chronic Diseases - LIDoC, Department of Physiological Sciences, Center of Biological Sciences, Federal University of Santa Catarina - UFSC, Florianópolis, Brazil.
Źródło:: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2021 Aug; Vol. 35 (8), pp. e21828.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
MeSH Terms:: Dexamethasone/*toxicity
Glucocorticoids/*toxicity
Insulin-Secreting Cells/*drug effects
Insulin-Secreting Cells/*physiology
Animals ; Animals, Genetically Modified ; Animals, Newborn ; Dexamethasone/administration & dosage ; Female ; Gene Expression Regulation/drug effects ; Glucocorticoids/administration & dosage ; Glucose Tolerance Test ; Insulin/pharmacology ; Mice ; Neoplasms, Experimental ; Pregnancy ; Prenatal Exposure Delayed Effects ; RNA, Messenger/genetics ; RNA, Messenger/metabolism
References:: Bonner-Weir S. Perspective: postnatal pancreatic beta cell growth. Endocrinology. 2000;141(6):1926-1939.
Parsons JA, Brelje TC, Sorenson RL. Adaptation of islets to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology. 1992;130:1459-1466.
Portha B, Levacher C, Picon L, et al. Diabetogenic effect of streptozotocin in the rat during the perinatal period. Diabetes. 1974;23(11):889-895.
Xu X, D’Hoker J, Stangé G, et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell. 2008;132(2):197-207.
Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest. 2007;117(9):2553-2561.
Wang RN, Bouwens L, Klöppel G. Beta-cell proliferation in normal and streptozotocin-treated newborn rats: site, dynamics and capacity. Diabetologia. 1994;37:1088-1096.
Guz Y, Nasir I, Teitelman G. Regeneration of pancreatic B-cells from intra-islet precursor cells in an experimental model of diabetes. Endocrinology. 2001;142:4956-4968.
Li L, Yi Z, Seno M, et al. Activin A and betacellulin: effect on regeneration of pancreatic beta-cells in neonatal streptozotocin-treated rats. Diabetes. 2004;53(3):608-615.
Chera S, Baronnier D, Ghila L, et al. Diabetes recovery by age-dependent conversion of pancreatic delta- cells into insulin producers. Nature. 2014;514(7523):503-507.
Thorel F, Népote V, Avril I, et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature. 2010;464(7292):1149-1154.
Kataoka M, Kawamuro Y, Shiraki N, et al. Recovery from diabetes in neonatal mice after a low dose streptozotocin treatment. Biochem Biophys Res Commun. 2013;430(3):1103-1108.
Rakieten N, Rakieten ML, Nadkarni MR. Studies on the diabetogenic action of streptozotocin (NSC-37917). Cancer Chemother Rep. 1963;29:91-98.
King R, Hill J, Saha B, et al. Offspring of mice exposed to a low-protein diet in utero demonstrate changes in mTOR signaling in pancreatic islets of langerhans, associated with altered glucagon and insulin expression and a lower β-cell mass. Nutrients. 2019;11(3):605.
Korchynska S, Krassnitzer M, Malenczyk K, et al. Life-long impairment of glucose homeostasis upon prenatal exposure to psychostimulants. EMBO J. 2020;39(1):e100882.
Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843.
Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976;295(7):349-353.
Moisiadis VG, Matthews SG. Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol. 2014;10(7):391-402.
Barker D, Osmond C, Winter PD, et al. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577-580.
Barker DJ. Adult consequences of fetal growth restriction. Clin Obstet Gynecol. 2006;49(2):270-283.
Franko KL, Forhead AJ, Fowden AL. Differential effects of prenatal stress and glucocorticoid administration on postnatal growth and glucose metabolism in rats. J Endocrinol. 2010;204(3):319-329.
O’Regan D, Kenyon CJ, Seckl JR, et al. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab. 2004;287(5):863-870.
Liggins GC, Howie RN. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics. 1972;50:515-525.
Nyirenda MJ, Lindsay RS, Kenyon CJ, et al. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest. 1998;101(10):2174-2181.
Pantaleão LC, Murata G, Teixeira CJ, et al. Prolonged fasting elicits increased hepatic triglyceride accumulation in rats born to dexamethasone-treated mothers. Sci Rep. 2017;7(1):10367.
de Vries A, Holmes MC, Heijnis A, et al. Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J Clin Invest. 2007;117(4):1058-1067.
Riveline J-P, Baz B, Nguewa J-L, et al. Exposure to glucocorticoids in the first part of fetal life is associated with insulin secretory defect in adult humans. J Clin Endocrinol Metab. 2020;105(3):e191-e199.
Protzek AO, Costa-Júnior JM, Rezende LF, et al. Augmented β-cell function and mass in glucocorticoid-treated rodents are associated with increased islet Ir-β/AKT/mTOR and decreased AMPK/ACC and AS160 signaling. Int J Endocrinol. 2014;2014:983453.
Thyssen S, Arany E, Hill DJ. Ontogeny of regeneration of beta-cells in the neonatal rat after treatment with streptozotocin. Endocrinology. 2006;147(5):2346-2356.
Santos CD, da Silva JS, Brunetta HS, et al. Impact of combined long-term fructose and prednisolone intake on glucose and lipid homeostasis in rats: benefits of intake interruption or fish oil administration. J Nutr Biochem. 2021;90:108572.
Chung C-H, Hao E, Piran R, et al. Pancreatic β-cell neogenesis by direct conversion from mature α-cells. Stem Cells. 2010;28(9):1630-1638.
Bacos K, Gillberg L, Volkov P, et al. Blood-based biomarkers of age-associated epigenetic changes in human islets associate with insulin secretion and diabetes. Nat Commun. 2016;7:11089.
Lundy BL, Jones NA, Field T, et al. Prenatal depression effects on neonates. Infant Behav Develop. 1999;22:121-137.
Blondeau B, Lesage J, Czernichow P, et al. Glucocorticoids impair fetal beta-cell development in rats. Am J Physiol Endocrinol Metab. 2001;281(3):E592-E599.
Karlsson L, Gezelius A, Nordenström A, et al. Cognitive impairment in adolescents and adults with congenital adrenal hyperplasia. Clin Endocrinol (Oxf). 2017;87(6):651-659.
Seckl JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol. 2004;151(3):U49-U62.
Bieswal F, Ahn M-T, Reusens B, et al. The importance of catch-up growth after early malnutrition for the programming of obesity in male rat. Obesity (Silver Spring). 2006;14(8):1330-1343.
Ozanne SE, Lewis R, Jennings BJ, et al. Early programming of weight gain in mice prevents the induction of obesity by a highly palatable diet. Clin Sci. 2004;106(2):141-145.
Godfrey KM, Costello PM, Lillycrop KA. Development, epigenetics and metabolic programming. Nestle Nutr Inst Workshop. 2016;85:71-80.
Feng AL, Xiang Y-Y, Gui LE, et al. Paracrine GABA and insulin regulate pancreatic alpha cell proliferation in a mouse model of type 1 diabetes. Diabetologia. 2017;60(6):1033-1042.
Aguayo-Mazzucato C, Bonner-Weir S. Pancreatic β-cell regeneration as a possible therapy for diabetes. Cell Metab. 2018;27(1):57-67.
Valtat B, Dupuis C, Zenaty D, et al. Genetic evidence of the programming of beta cell mass and function by glucocorticoids in mice. Diabetologia. 2011;54(2):350-359.
Müller TD, Finan B, Bloom SR, et al. Glucagon-like peptide 1 (GLP-1). Mol Metab. 2019;30:72-130.
Wang RN, Bouwens L, Klöppel G. Beta-cell growth in adolescent and adult rats treated with streptozotocin during the neonatal period. Diabetologia. 1996;39(5):548-557.
Movassat J, Portha B. Beta-cell growth in the neonatal Goto-Kakisaki rat and regeneration after treatment with streptozotocin at birth. Diabetologia. 1999;42(9):1098-1106.
Goyal D, Limesand SW, Goyal R. Epigenetic responses and the developmental origins of health and disease. J Endocrinol. 2019;242(1):T105-T119.
Chen Y-T, Hu Y, Yang Q-Y, et al. Excessive glucocorticoids during pregnancy impair fetal brown fat development and predispose offspring to metabolic dysfunctions. Diabetes. 2020;69(8):1662-1674.
Sandovici I, Smith NH, Nitert MD, et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc Natl Acad Sci U S A. 2011;108(13):5449-5454.
Wang Z, Gleichmann H. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes. 1998;47(1):50-56.
Contributed Indexing:: Keywords: Hnf4-α; beta-cell regeneration; glucocorticoid; low birth weight; offspring
Substance Nomenclature:: 0 (Glucocorticoids)
0 (Insulin)
0 (RNA, Messenger)
7S5I7G3JQL (Dexamethasone)
Entry Date(s):: Date Created: 20210729 Date Completed: 20210810 Latest Revision: 20210810
Update Code:: 20240105
DOI:: 10.1096/fj.202100841R
PMID:: 34325494
: Czasopismo naukowe

Since prenatal glucocorticoids (GC) excess increases the risk of metabolic dysfunctions in the offspring and its effect on β-cell recovery capacity remains unknown we investigated these aspects in offspring from mice treated with dexamethasone (DEX) in the late pregnancy. Half of the pups were treated with streptozotocin (STZ) on the sixth postnatal day (PN). Functional and molecular analyses were performed in male offspring on PN25 and PN225. Prenatal DEX treatment resulted in low birth weight. At PN25, both the STZ-treated offspring developed hyperglycemia and had lower β-cell mass, in parallel with higher α-cell mass and glucose intolerance, with no impact of prenatal DEX on such parameters. At PN225, the β-cell mass was partially recovered in the STZ-treated mice, but they remained glucose-intolerant, irrespective of being insulin sensitive. Prenatal exposition to DEX predisposed adult offspring to sustained hyperglycemia and perturbed islet function (lower insulin and higher glucagon response to glucose) in parallel with exacerbated glucose intolerance. β-cell-specific knockdown of the Hnf4α in mice from the DS group resulted in exacerbated glucose intolerance. We conclude that high GC exposure during the prenatal period exacerbates the metabolic dysfunctions in adult life of mice exposed to STZ early in life, resulting in a lesser ability to recover the islets' function over time. This study alerts to the importance of proper management of exogenous GCs during pregnancy and a healthy postnatal lifestyle since the combination of adverse factors during the prenatal and postnatal period accentuates the predisposition to metabolic disorders in adult life.
(© 2021 Federation of American Societies for Experimental Biology.)

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