Gestational hyperglycemia reprograms cardiac gene expression in rat offspring
Abstract
BackgroundRat fetuses with maternal pregestational hyperglycemia develop cardiac dysfunction, and their cardiac gene expression differs from that of healthy control fetuses near term. We hypothesized that cardiac gene expression and morphologic abnormalities of rat fetuses with maternal pregestational hyperglycemia become normal after birth.MethodsNine rats were preconceptually injected with streptozotocin to induce maternal hyperglycemia and nine rats served as controls. The hyperglycemia group comprised 82 mice and the control group 74 offspring fed by euglycemic dams. Hearts of the offspring were collected on postnatal days 0, 7, and 14, and processed for histologic and gene expression analyses.ResultsOn day 0, heart weight was increased, and expression of cardiac genes involved in contractility, growth, and metabolism was decreased in the hyperglycemia group. On day 7, although cardiomyocyte apoptosis was enhanced, most of the changes in gene expression had normalized in the hyperglycemia group. By day 14, the expression of genes important for myocardial growth, function, and metabolism was again abnormal in the hyperglycemia group.ConclusionMost cardiac gene expression abnormalities become transiently normal during the first week of life of offspring to hyperglycemic rats. However, by day 14, cardiac expressions of genes involved in growth, function, and metabolism are again abnormal in relation to control offspring.
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Maternal hyperglycemia reprograms cardiac gene expression in fetal rat offspring.
“Maternal hyperglycemia also reprogrammed cardiac gene expression in fetal rat offspring, with genes involved in myocardial growth, contraction and metabolism most prominently affected [118].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [118]
Genes involved in myocardial growth, contraction and metabolism are most prominently affected in fetal rat offspring after maternal hyperglycemia.
“Maternal hyperglycemia also reprogrammed cardiac gene expression in fetal rat offspring, with genes involved in myocardial growth, contraction and metabolism most prominently affected [118].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [118]
Cites
Diabetogenic action of streptozotocin: relationship of dose to metabolic response
Junod, A. F., Lambert, A. E., Stauffacher, W., & Renold, A. E. (1969) · Journal of Clinical Investigation · doi:10.1172/jci106180 · Cited by 931 · see citing works
Shimada, H., Chatten, J., Newton, W. A., Sachs, N., Hamoudi, A. B., Chiba, T., Marsden, H. B., & Misugi, K. (1984) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/73.2.405 · Cited by 858 · see citing works
Rapid Transition of Cardiac Myocytes from Hyperplasia to Hypertrophy During Postnatal Development
Li, F. (1996) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1996.0163 · Cited by 837 · see citing works
Animal models of diabetes mellitus
Rees, A., & Alcolado, J. C. (2005) · Diabetic Medicine · doi:10.1111/j.1464-5491.2005.01499.x · Cited by 735 · see citing works
Structural Aspects of Postnatal Lung Development – Alveolar Formation and Growth
Burri, P. H. (2006) · Neonatology · doi:10.1159/000092868 · Cited by 487 · see citing works
Effects of diabetic pregnancy on the fetus and newborn
Schwartz, R., & Teramo, K. (2000) · Seminars in Perinatology · doi:10.1053/sp.2000.6363 · Cited by 451 · see citing works
Return to the fetal gene program protects the stressed heart: a strong hypothesis
Rajabi, M., Kassiotis, C., Razeghi, P., & Taegtmeyer, H. (2007) · Heart Failure Reviews · doi:10.1007/s10741-007-9034-1 · Cited by 425 · see citing works
Nold, J. L., & Georgieff, M. (2004) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2004.01.003 · Cited by 299 · see citing works
Signaling Pathways in Cardiac Myocyte Hypertrophy
Hefti, M. A., Harder, B. A., Eppenberger, H. M., & SCHAUB, M. C. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0523 · Cited by 241 · see citing works
The offspring of the diabetic mother – Short- and long-term implications
Mitanchez, D., Yzydorczyk, C., Siddeek, B., Boubred, F., Benahmed, M., & Siméoni, U. (2014) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2014.08.004 · Cited by 223 · see citing works
Cole, M. A., Murray, A. J., Cochlin, L. E., Heather, L. C., McAleese, S., Knight, N. S., Sutton, E. R., Jamil, A. H. A., Parassol, N., & Clarke, K. (2011) · Basic Research in Cardiology · doi:10.1007/s00395-011-0156-1 · Cited by 190 · see citing works
Regulation of the cardiomyocyte population in the developing heart
Thornburg, K. L. R., Jonker, S. S., O'Tierney, P. F., Chattergoon, N. N., Louey, S., Faber, J., & Giraud, G. D. (2010) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2010.11.010 · Cited by 100 · see citing works
Sisino, G., Bouckenooghe, T., Aurientis, S., Fontaine, P., Storme, L., & Vambergue, A. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.07.009 · Cited by 99 · see citing works
Postnatal development of mouse heart: formation of energetic microdomains
Piquereau, J., Novotová, M., Fortin, D., Garnier, A., Ventura‐Clapier, R., Veksler, V., & Joubert, F. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.189670 · Cited by 95 · see citing works
Apoptotic cardiomyocyte death in fatal myocarditis.
Kytö, V., Saraste, A., Saukko, P., Henn, V., Pulkki, K., Vuorinen, T., & Voipio-Pulkki, L. (2004) · American Journal of Cardiology · doi:10.1016/j.amjcard.2004.05.056 · Cited by 83 · see citing works
Self-citationMaternal Diabetes In Vivo and High Glucose In Vitro Diminish GAPDH Activity in Rat Embryos
Wentzel, P., Ejdesjö, A., & Eriksson, U. J. (2003) · Diabetes · doi:10.2337/diabetes.52.5.1222 · Cited by 81 · see citing works
Gene Structure of a New Cardiac Peptide Hormone: A Model for Heart-Specific Gene Expression1
Majalahti-Palviainen, T., Hirvinen, M., Tervonen, V., Ilves, M., Ruskoaho, H. J., & Vuolteenaho, O. J. (2000) · Endocrinology · doi:10.1210/endo.141.2.7312 · Cited by 81 · see citing works
Self-citationUncoupling Proteins: Role in Insulin Resistance and Insulin Insufficiency
B.Chan, C., & Harper, M.-E. (2006) · Current Diabetes Reviews · doi:10.2174/157339906777950660 · Cited by 71 · see citing works
Hyperinsulinemic Hypoglycemia – The Molecular Mechanisms
Nessa, A., Rahman, S. A., & Hussain, K. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00029 · Cited by 66 · see citing works
Interventricular septal thickness in fetuses of diabetic mothers.
Veille, J.-C., Sivakoff, M. C., Hanson, R., & Fanaroff, A. A. (1992) · PubMed · Cited by 64 · see citing works
Åman, J., Hansson, U., Östlund, I., Wall, K., & Persson, B. (2011) · Neonatology · doi:10.1159/000323741 · Cited by 60 · see citing works
Oberhoffer, R., Högel, J., Stoz, F., KOHNE, E., & Lang, D. (1997) · European Journal of Pediatrics · doi:10.1007/s004310050596 · Cited by 52 · see citing works
Kantor, P. F., Robertson, M. A., Coe, J. Y., & Lopaschuk, G. D. (1999) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(99)00063-7 · Cited by 50 · see citing works
Lipopolysaccharide induced apoptosis of rat pancreatic acinar cells.
Laine, V. J. O., Nyman, K., Peuravuori, H. J., Henriksén, K., Parvinen, M., & Nevalainen, T. J. (1996) · Gut · doi:10.1136/gut.38.5.747 · Cited by 48 · see citing works
Rat maternal diabetes impairs pancreatic β-cell function in the offspring
Han, J., Xu, J., Long, Y. S., Epstein, P. N., & Liu, Y. Q. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00479.2006 · Cited by 45 · see citing works
Maternal hyperglycemia leads to fetal cardiac hyperplasia and dysfunction in a rat model
Lehtoranta, L., Vuolteenaho, O. J., Laine, V. J. O., Koskinen, A., Soukka, H., Kytö, V., Määttä, J. A., Haapsamo, M., Ekholm, E. M. K., & Rasanen, J. P. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00043.2013 · Cited by 39 · see citing works
Self-citationHeart disease in infants of diabetic mothers.
Narchı, H., & Kulaylat, N. A. (2000) · PubMed · Cited by 35 · see citing works
Revuelta‐López, E., Cal, R., Herraiz‐Martínez, A., de Gonzalo‐Calvo, D., Nasarre, L., Roura, S., Gálvez‐Montón, C., Bayés‐Genís, A., Badimón, L., Hove‐Madsen, L., et al. (2015) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2015.04.028 · Cited by 23 · see citing works
Vessières, E., Dib, A., Bourreau, J., Lelièvre, E., Custaud, M., Lelièvre-Pégorier, M., Loufrani, L., Henrion, D., & Fassot, C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146830 · Cited by 18 · see citing works
Cardiomyopathy and Diastolic Dysfunction in the Embryo and Neonate of a Type 1 Diabetic Mouse Model
Corrigan, N., Treacy, A. D., Brazil, D. P., & McAuliffe, F. M. (2012) · Reproductive Sciences · doi:10.1177/1933719112466298 · Cited by 16 · see citing works
Lehtoranta, L., Vuolteenaho, O. J., Laine, J., Polari, L., Ekholm, E. M. K., & Rasanen, J. P. (2016) · Placenta · doi:10.1016/j.placenta.2016.06.002 · Cited by 12 · see citing works
Self-citationStereology of the Myocardium in Embryos, Fetuses and Neonates of the Rat
Mandarim‐de‐Lacerda, C. A., & Pessanha, M. G. (1995) · Cells Tissues Organs · doi:10.1159/000147777 · Cited by 12 · see citing works
Stereological and Histological Analysis of the Developing Rat Heart
Altunkaynak, M. E., Altunkaynak, B. Z., Ünal, D., Yıldırım, S., Can, I., & Ünal, B. (2011) · Anatomia Histologia Embryologia · doi:10.1111/j.1439-0264.2011.01085.x · Cited by 6 · see citing works
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Sorted by citations
Kereliuk, S. M., & Dolinsky, V. W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084467 · Cited by 34 · see citing works
“Maternal hyperglycemia also reprogrammed cardiac gene expression in fetal rat offspring, with genes involved in myocardial growth, contraction and metabolism most prominently affected [118].”
BackgroundKostina, A. S., Lewis‐Israeli, Y. R., Abdelhamid, M., Gabalski, M. A., Kiselev, A. M., Volmert, B. D., Lankerd, H., Huang, A., Wasserman, A. H., Lydic, T. A., et al. (2024) · Stem Cell Reports · doi:10.1016/j.stemcr.2024.01.003 · Cited by 36 · see citing works
Armengaud, J.-B., Ronald, C. W., Siddeek, B., Visser, G. H. A., & Siméoni, U. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.07.039 · Cited by 31 · see citing works
Lewis‐Israeli, Y. R., Abdelhamid, M., Olomu, I. N., & Aguirre, A. (2022) · Current Protocols · doi:10.1002/cpz1.461 · Cited by 20 · see citing works
Schütte, T., Kedziora, S. M., Haase, N., Herse, F., Alenina, N. V., Müller, D. N., Bäder, M., Schupp, M., Dechend, R., Golić, M., et al. (2021) · Diabetologia · doi:10.1007/s00125-021-05566-5 · Cited by 8 · see citing works
Kostina, A. S., Lewis‐Israeli, Y. R., Abdelhamid, M., Gabalski, M. A., Volmert, B. D., Lankerd, H., Huang, A., Wasserman, A. H., Lydic, T. A., Chan, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.07.544081 · Cited by 7 · see citing works
Peng, Y., Feng, W. S., Wei, Z., Liao, X., Yang, H., Chang, C., Gan, L., & Zhang, J. (2024) · Early Human Development · doi:10.1016/j.earlhumdev.2024.106168 · Cited by 5 · see citing works
Pereira, M. M. D. S., de Melo, I. M. F., Braga, V. A. Á., Teixeira, Á. A. C., & Teixeira, V. W. (2022) · Histochemistry and Cell Biology · doi:10.1007/s00418-021-02069-7 · Cited by 5 · see citing works
Melatonin Administration Prevents Placental and Fetal Changes Induced by Gestational Diabetes
de Melo, I. M. F., Ferreira, C. G. M., Alves, É. R., D’assunção, C. G., Neto, C. J. C. L., de Albuquerque, Y. M. L., Teixeira, V. W., & Teixeira, Á. A. C. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-00850-0 · Cited by 5 · see citing works
- Authors
- Lehtoranta, L., Koskinen, A., Vuolteenaho, O., Laine, J., Kytö, V., Soukka, H., Ekholm, E., & Räsänen, J.
- Affiliations
- University of Turku (FI)
- Corresponding author
- Lehtoranta, Lara
- Venue
- Pediatric Research
- Published
- 2017-05-31
- Volume
- 82
- Issue
- 2
- Pages
- 356-361
- ISSN
- 0031-3998 (ISSN-L)
- 1530-0447
- OpenAlex
- W2596518609
- Cited by
- 9
- References
- 33
- Citations by year
- 2024: 2 · 2023: 1 · 2022: 4 · 2021: 1 · 2018: 1
- FWCI
- 0.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pediatric Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- hyperglycemia in pregnancy, cardiac gene expression, fetal heart, cardiomyocyte apoptosis, myocardial growth, myocardial metabolism, postnatal development, streptozotocin-induced diabetes, diabetic cardiomyopathy
- MeSH terms
- Animals, Body Weight, Female, Hyperglycemia, Myocardium, Organ Size, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Streptozocin, Gene Expression, Diabetes, Gestational, Reverse Transcriptase Polymerase Chain Reaction, Rats
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