Influence of maternal hyperglycemia on rat daughters and granddaughters
DOI:
https://doi.org/10.33448/rsd-v12i6.41798Keywords:
Diabetes; Rats; Reproductive outcomes; Fetus; Pregnancy.Abstract
This study evaluated the influence of maternal diabetes on the reproductive outcomes of adult daughters during full-term pregnancy in rats. The local ethics committee approved all experimental protocols. The adult female pups of nondiabetic (control – CP) and diabetic (DP) mothers were subjected to mating with healthy male rats for reproductive analysis. On day 17 of pregnancy, both groups underwent an oral glucose tolerance test (OGTT) to evaluate glucose tolerance. At the end of pregnancy, the rats were anesthetized for laparotomy and exposure of maternal organs. Uterine horns, ovaries, fetuses, and placentas were weighed to classify fetal weight and placental efficiency. P<0.05 was considered a statistically significant limit, and Pearson's correlation was used. Higher maternal fasting blood glucose was correlated with a lower number of live fetuses and, consequently, with a lower litter weight. Thus, maternal fasting glucose during pregnancy is a relevant biomarker related to the poor reproductive outcome of daughters of rats. Furthermore, these findings show the detrimental effects of fetal programming induced by maternal diabetes in adulthood in the subsequent generation.
References
ADA. (2022). Classification and diagnosis of diabetes. Diabetes Care. 44: S15–S33.
Barco, V. S., Gallego, F. Q., Paula, V. G., Cruz, L. L., Karki, B., Volpato, G. T. & Damasceno D. C. (2022). Effects of diabetes between generations on the pre-embryos of rats. An Acad Bras Ciênc. 94:e20220717.
Beery, A. K. & Francis, D. D. (2011). Adaptive significance of natural variations in maternal care in rats: a translational perspective. Neurosci Biobehav Rev. 35(7):1552–1561.
Bueno, A., Sinzato, Y. K., Volpato, G. T., Gallego, F. Q., Perecin, F., Rodrigues, T. & Damasceno, D. C. (2020). Severity of prepregnancy diabetes on the fetal malformations and viability associated with early embryos in rats. Biol Reprod. 103: 938-950.
Champagne, F. A., Francis, D. D., Mar, A. & Meaney, M. J. (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav. 79(3):359–371.
Damasceno, D. C., Kiss, A. C. I., Sinzato, Y. K., De Campos, K. E., Rudge, M. V. C., Calderon, I. M. P. & Volpato, G. T. (2011). Maternal fetal outcome, lipid profile and oxidative stress of diabetic rats neonatally exposed to streptozotocin. Exp Clin Endocrinol Diabetes. 7:408–413.
Damasceno, D. C., Sinzato, Y. K., Bueno, A., Netto, A.O., Dallaqua, B., Gallego, F. Q., Iessi I. L., Corvino, S. B., Serrano, R. G., Marini, G., Piculo, F., Calderon, I. M. & Rudge, M. V. (2013). Mild diabetes models and their maternal-fetal repercussions. J Diabetes Res. 2013: 473575.
Damasceno, D. C., Volpato, G. T., Calderon, I. M. P. & Rudge, M. V. C. (2002). Oxidative stress and diabetes in pregnant rats. Anim Reprod Sci. 72: 235 – 244.
Gallego, F. Q., Miranda, C. A., Sinzato, Y. K., Iessi, I. L., Dallaqua, B., Pando, R. H., Rocha, N. S., Volpato, G. T. & Damasceno, D. C. (2019). Temporal analysis of distribution pattern of islet cells and antioxidant enzymes for diabetes onset in postnatal critical development window in rats. Life Sci. 226:57–67.
Herrera, E. & Amusquivar, E. (2000). Lipid metabolism in the fetus and the newborn. Diabetes Metab Res Rev. 16: 202–10.
Hufnagel, A., Dearden, L., Fernandez-Twinn, D. S. & Ozanne, S. E. (2022). Programming of cardiometabolic health: the role of maternal and fetal hyperinsulinaemia. The Journal of Endocrinology. 253(2), R47.
internacional society for developmental origins of health and disease. (2023). The DOHaD Story. Impact. https://dohadsoc.org/impact/
Klöppel, E., Sinzato, Y. K., Rodrigues, T., Gallego, F. Q., Karki, B., Volpato, G. T., Corrente, J. E., Roy, S. & Damasceno, D. C. (2023). Benefits of Vitamin D supplementation on pregnancy of rats with pregestational diabetes and their offspring. Reprod Sci. 30:In press.
Lowe, W. L. Jr., Lowe, L. P., Kuang, A., Catalano, P. M., Nodzenski, M., Talbot, O., Tam, W., Sacks, D. A., McCance, D., Linder, B., Lebenthal, Y., Lawrence, J. M., Lashley, M., Josefson, J. L., Hamilton, J., Deerochanawong, C., Clayton, P., Brickman, W. J., Dyer, A. R., Scholtens, D. M., Metzger, B. E., & HAPO Follow-up Study Cooperative Research Group. (2019). Maternal glucose levels during pregnancy and childhood adiposity in the Hyperglycemia and Adverse Pregnancy Outcome Follow-up Study. Diabetologia. 62:598–610.
Moraes-souza, R. Q., Soares, T. S., Carmo, N. O., Damasceno, D. C., Campos, K. E. & Volpato, G. T. (2017). Adverse effects of Croton urucurana B. exposure during rat pregnancy. J Ethnopharmacol. 199:328-333.
Ornoy, A., Becker, M., Weinstein-Fudim, L. & Ergaz, Z. (2021). Diabetes during pregnancy: A maternal disease complicating the course of pregnancy with long-term deleterious effects on the offspring. a clinical review. International Journal of Molecular Sciences. 22(6), 2965.
Paula, V. G., Sinzato, Y. K., De Moraes-souza, R. Q., Soares, T. S., Souza, F. Q. G., Karki, B., De andrade paes, A. M., Corrente, J. E., Damasceno, D. C., & Volpato, G. T. (2022). Metabolic changes in female rats exposed to intrauterine hyperglycemia and postweaning consumption of high-fat diet. Biol Reprod. 106(1): 200-212.
Simpson, J. & Kelly, J. P. (2011). The impact of environmental enrichment in laboratory rats—behavioral and neurochemical aspects. Behav Brain Res. 222:246–264.
Sinzato, Y. K., Klöppel, E., Miranda, C. A., Paula, V. G., Alves, L. F., Nascimento, L. L., Campos, A. P., Karki, B., Hampl, V., Volpato, G. T., & Damasceno, D. C. (2021). Comparison of streptozotocin-induced diabetes at different moments of the life of female rats for translational studies. Lab Anim. 55: 329-340.
Sinzato, Y. K., Paula, V. G., Gallego, F. Q., Moraes-souza, R. Q., Corrente, J. E., Volpato, G. T. & Damasceno, D. C. (2022). Maternal diabetes and postnatal high-fat diet on pregnant offspring. Front Cell Dev Biol. 10: 818621.
Sun, H., Saeedi, P., Karuranga, S., Pinkepank, M., Ogurtsova, K., Duncan, B. B., Stein, C., Basit, A., Chan, J. C. N., Mbanya, J. C., Pavkov, M. E., Ramachandaran, A., Wild, S. H., James, S., Herman, W. H., Zhang, P., Bommer, C., Kuo, S., Boyko, E. J. & Magliano, D. J. (2022). IDF Diabetes Atlas: global, regional, and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 183:109119.
Tai, M. M. (1994). A mathematical model for the determination of total area under glucose tolerance and other metabolic curves. Diabetes Care. 17:152-154.
Yang, X., Hu, R., Shi, M., Wang, L., Yan, J., Gong, J., Zhang, Q., He, J. & Wu, S. (2023). Placental Malfunction, Fetal Survival and Development Caused by Sow Metabolic Disorder: The Impact of Maternal Oxidative Stress. Antioxidants. 12(2), 360.
Zheng, X., Narayanan, S., Xu, C., Angelstig, S. E., Grünler, J., Zhao, A., Di Toro, A., Bernardi, L., Mazzone, M., Carmeliet, P., Del Sole, M., Solaini, G., Fosberg, E. A., Zhang, A., Brismar, K., Schiffer, T. A., Ekberg, N. R., Botusan, I. R., Palm, F. & Catrina, S. B. (2022). Repression of hypoxia-inducible factor-1 contributes to increased mitochondrial reactive oxygen species production in diabetes. elife, 11, e70714.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Luigi M. Jeuken Di Domizio; Maria Eduarda Picolo Gomes; Verônyca Gonçalves Paula; Maysa Rocha de Souza; Franciane Quintanilha Gallego; Vinícius Soares Barco; Débora Cristina Damasceno
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
