Skip to main content
main-content
Erschienen in: Cardiovascular Toxicology 9/2022

28.07.2022

Maternal Ethanol Exposure-Induced Cardiac Fibrosis is Associated with Changes in TGF-β and SIRT1/FOXO3a Signaling in Male Rat Offspring: A Three-Month Follow-up Study

verfasst von: Alireza Shirpoor, Roya Naderi

Erschienen in: Cardiovascular Toxicology | Ausgabe 9/2022

Einloggen, um Zugang zu erhalten

Abstract

Ethanol exposure during pregnancy induces cardiac fibrosis in the fetal heart. However, the mechanisms by which consumption of ethanol induces fibrotic changes are not known. Pregnant rats were received ethanol 4.5 g/kg BW once per day from the 7th day of pregnancy (GD7) throughout lactation. Our findings demonstrated that, area of fibrosis increased in cardiac tissue in the pups on both postnatal day twenty one (PN21) and postnatal day ninety (PN90) after prenatal and early postnatal period ethanol treatment compared with the controls. It was accompanied by a decline in the expression of SIRT1 protein along with the elevation of FOXO3a and TGF-β protein expressions which were determined by western blot. Overall, our data reveal that prenatal alcohol usage increase in fibrotic regions in the pup hearts possibly by regulating TGF-β, FOXO3a and SIRT1 protein levels. These are potential therapeutic molecular targets that can be modulated to protect heart against maternal ethanol exposure.
Literatur
1.
Zurück zum Zitat Jones, K. L., & Smith, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet (London, England), 302(7836), 999–1001. CrossRef Jones, K. L., & Smith, D. W. (1973). Recognition of the fetal alcohol syndrome in early infancy. Lancet (London, England), 302(7836), 999–1001. CrossRef
2.
Zurück zum Zitat Henderson, G. I., Devi, B. G., Perez, A., & Schenker, S. (1995). In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcoholism, Clinical and Experimental Research, 19(3), 714–720. PubMedCrossRef Henderson, G. I., Devi, B. G., Perez, A., & Schenker, S. (1995). In utero ethanol exposure elicits oxidative stress in the rat fetus. Alcoholism, Clinical and Experimental Research, 19(3), 714–720. PubMedCrossRef
3.
Zurück zum Zitat Daft, P. A., Johnston, M. C., & Sulik, K. K. (1986). Abnormal heart and great vessel development following acute ethanol exposure in mice. Teratology, 33(1), 93–104. PubMedCrossRef Daft, P. A., Johnston, M. C., & Sulik, K. K. (1986). Abnormal heart and great vessel development following acute ethanol exposure in mice. Teratology, 33(1), 93–104. PubMedCrossRef
4.
Zurück zum Zitat Shirpoor, A., Gaderi, R., & Naderi, R. (2019). Ethanol exposure in prenatal and early postnatal induced cardiac injury in rats: Involvement of oxidative stress, Hsp70, ERK 1/2, JNK, and apoptosis in a 3-month follow-up study. Cell Stress & Chaperones, 24(5), 917–926. CrossRef Shirpoor, A., Gaderi, R., & Naderi, R. (2019). Ethanol exposure in prenatal and early postnatal induced cardiac injury in rats: Involvement of oxidative stress, Hsp70, ERK 1/2, JNK, and apoptosis in a 3-month follow-up study. Cell Stress & Chaperones, 24(5), 917–926. CrossRef
5.
Zurück zum Zitat Patel, V. B., Why, H. J., Richardson, P. J., & Preedy, V. R. (1997). The effects of alcohol on the heart. Adverse Drug Reactions and Toxicological Reviews, 16(1), 15–43. PubMed Patel, V. B., Why, H. J., Richardson, P. J., & Preedy, V. R. (1997). The effects of alcohol on the heart. Adverse Drug Reactions and Toxicological Reviews, 16(1), 15–43. PubMed
6.
7.
Zurück zum Zitat Zhou, C., Huang, J., Li, Q., Zhan, C., He, Y., Liu, J., et al. (2018). Pharmacological inhibition of soluble epoxide hydrolase ameliorates chronic ethanol-Induced cardiac fibrosis by restoring autophagic flux. Alcoholism, Clinical and Experimental Research, 42(10), 1970–1978. PubMedCrossRef Zhou, C., Huang, J., Li, Q., Zhan, C., He, Y., Liu, J., et al. (2018). Pharmacological inhibition of soluble epoxide hydrolase ameliorates chronic ethanol-Induced cardiac fibrosis by restoring autophagic flux. Alcoholism, Clinical and Experimental Research, 42(10), 1970–1978. PubMedCrossRef
8.
Zurück zum Zitat Ma, Z., Zang, W., Wang, H., & Wei, X. (2020). Silibinin enhances anti-renal fibrosis effect of MK-521 via downregulation of TGF-β signaling pathway. Human Cell, 33(2), 330–336. PubMedCrossRef Ma, Z., Zang, W., Wang, H., & Wei, X. (2020). Silibinin enhances anti-renal fibrosis effect of MK-521 via downregulation of TGF-β signaling pathway. Human Cell, 33(2), 330–336. PubMedCrossRef
9.
Zurück zum Zitat Gaitantzi, H., Meyer, C., Rakoczy, P., Thomas, M., Wahl, K., Wandrer, F., et al. (2018). Ethanol sensitizes hepatocytes for TGF-β-triggered apoptosis. Cell Death & Disease, 9(2), 51. CrossRef Gaitantzi, H., Meyer, C., Rakoczy, P., Thomas, M., Wahl, K., Wandrer, F., et al. (2018). Ethanol sensitizes hepatocytes for TGF-β-triggered apoptosis. Cell Death & Disease, 9(2), 51. CrossRef
10.
Zurück zum Zitat Uesugi, T., Froh, M., Gäbele, E., Isayama, F., Bradford, B. U., Ikai, I., et al. (2004). Contribution of angiotensin II to alcohol-induced pancreatic fibrosis in rats. The Journal of Pharmacology and Experimental Therapeutics, 311(3), 921–928. PubMedCrossRef Uesugi, T., Froh, M., Gäbele, E., Isayama, F., Bradford, B. U., Ikai, I., et al. (2004). Contribution of angiotensin II to alcohol-induced pancreatic fibrosis in rats. The Journal of Pharmacology and Experimental Therapeutics, 311(3), 921–928. PubMedCrossRef
11.
Zurück zum Zitat Singhal, P. C., Reddy, K., Ding, G., Kapasi, A., Franki, N., Ranjan, R., et al. (1999). Ethanol-induced macrophage apoptosis: The role of TGF-beta. Journal of Immunology, 162(5), 3031–3036. Singhal, P. C., Reddy, K., Ding, G., Kapasi, A., Franki, N., Ranjan, R., et al. (1999). Ethanol-induced macrophage apoptosis: The role of TGF-beta. Journal of Immunology, 162(5), 3031–3036.
12.
Zurück zum Zitat Law, B. A., & Carver, W. E. (2013). Activation of cardiac fibroblasts by ethanol is blocked by TGF-β inhibition. Alcoholism, Clinical and Experimental Research, 37(8), 1286–1294. PubMedPubMedCentralCrossRef Law, B. A., & Carver, W. E. (2013). Activation of cardiac fibroblasts by ethanol is blocked by TGF-β inhibition. Alcoholism, Clinical and Experimental Research, 37(8), 1286–1294. PubMedPubMedCentralCrossRef
13.
Zurück zum Zitat Alcendor, R. R., Gao, S., Zhai, P., Zablocki, D., Holle, E., Yu, X., et al. (2007). Sirt1 regulates aging and resistance to oxidative stress in the heart. Circulation Research, 100(10), 1512–1521. PubMedCrossRef Alcendor, R. R., Gao, S., Zhai, P., Zablocki, D., Holle, E., Yu, X., et al. (2007). Sirt1 regulates aging and resistance to oxidative stress in the heart. Circulation Research, 100(10), 1512–1521. PubMedCrossRef
14.
Zurück zum Zitat Ninh, V. K., El Hajj, E. C., Ronis, M. J., & Gardner, J. D. (2019). N-Acetylcysteine prevents the decreases in cardiac collagen I/III ratio and systolic function in neonatal mice with prenatal alcohol exposure. Toxicology Letters, 315, 87–95. PubMedPubMedCentralCrossRef Ninh, V. K., El Hajj, E. C., Ronis, M. J., & Gardner, J. D. (2019). N-Acetylcysteine prevents the decreases in cardiac collagen I/III ratio and systolic function in neonatal mice with prenatal alcohol exposure. Toxicology Letters, 315, 87–95. PubMedPubMedCentralCrossRef
15.
Zurück zum Zitat Pulla, V. K., Battu, M. B., Alvala, M., Sriram, D., & Yogeeswari, P. (2012). Can targeting SIRT-1 to treat type 2 diabetes be a good strategy? A review. Expert Opinion on Therapeutic Targets, 16(8), 819–832. PubMedCrossRef Pulla, V. K., Battu, M. B., Alvala, M., Sriram, D., & Yogeeswari, P. (2012). Can targeting SIRT-1 to treat type 2 diabetes be a good strategy? A review. Expert Opinion on Therapeutic Targets, 16(8), 819–832. PubMedCrossRef
16.
Zurück zum Zitat Yang, J., Wang, N., Zhu, Y., & Feng, P. (2011). Roles of SIRT1 in high glucose-induced endothelial impairment: Association with diabetic atherosclerosis. Archives of Medical Research, 42(5), 354–360. PubMedCrossRef Yang, J., Wang, N., Zhu, Y., & Feng, P. (2011). Roles of SIRT1 in high glucose-induced endothelial impairment: Association with diabetic atherosclerosis. Archives of Medical Research, 42(5), 354–360. PubMedCrossRef
17.
Zurück zum Zitat Xie, J., Zhang, X., & Zhang, L. (2013). Negative regulation of inflammation by SIRT1. Pharmacological Research, 67(1), 60–67. PubMedCrossRef Xie, J., Zhang, X., & Zhang, L. (2013). Negative regulation of inflammation by SIRT1. Pharmacological Research, 67(1), 60–67. PubMedCrossRef
18.
Zurück zum Zitat Samuel, S. M., Thirunavukkarasu, M., Penumathsa, S. V., Paul, D., & Maulik, N. (2008). Akt/FOXO3a/SIRT1-mediated cardioprotection by n-tyrosol against ischemic stress in rat in vivo model of myocardial infarction: Switching gears toward survival and longevity. Journal of Agricultural and Food Chemistry, 56(20), 9692–9698. PubMedPubMedCentralCrossRef Samuel, S. M., Thirunavukkarasu, M., Penumathsa, S. V., Paul, D., & Maulik, N. (2008). Akt/FOXO3a/SIRT1-mediated cardioprotection by n-tyrosol against ischemic stress in rat in vivo model of myocardial infarction: Switching gears toward survival and longevity. Journal of Agricultural and Food Chemistry, 56(20), 9692–9698. PubMedPubMedCentralCrossRef
19.
Zurück zum Zitat Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science (New York, NY), 303(5666), 2011–2015. CrossRef Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., et al. (2004). Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science (New York, NY), 303(5666), 2011–2015. CrossRef
20.
Zurück zum Zitat Langley, E., Pearson, M., Faretta, M., Bauer, U. M., Frye, R. A., Minucci, S., et al. (2002). Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. The EMBO Journal, 21(10), 2383–2396. PubMedPubMedCentralCrossRef Langley, E., Pearson, M., Faretta, M., Bauer, U. M., Frye, R. A., Minucci, S., et al. (2002). Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. The EMBO Journal, 21(10), 2383–2396. PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Yeung, F., Hoberg, J. E., Ramsey, C. S., Keller, M. D., Jones, D. R., Frye, R. A., et al. (2004). Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. The EMBO Journal, 23(12), 2369–2380. PubMedPubMedCentralCrossRef Yeung, F., Hoberg, J. E., Ramsey, C. S., Keller, M. D., Jones, D. R., Frye, R. A., et al. (2004). Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. The EMBO Journal, 23(12), 2369–2380. PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Motta, M. C., Divecha, N., Lemieux, M., Kamel, C., Chen, D., Gu, W., et al. (2004). Mammalian SIRT1 represses forkhead transcription factors. Cell, 116(4), 551–563. PubMedCrossRef Motta, M. C., Divecha, N., Lemieux, M., Kamel, C., Chen, D., Gu, W., et al. (2004). Mammalian SIRT1 represses forkhead transcription factors. Cell, 116(4), 551–563. PubMedCrossRef
23.
Zurück zum Zitat Huang, H., & Tindall, D. J. (2007). Dynamic FoxO transcription factors. Journal of Cell Science, 120(Pt 15), 2479–2487. PubMedCrossRef Huang, H., & Tindall, D. J. (2007). Dynamic FoxO transcription factors. Journal of Cell Science, 120(Pt 15), 2479–2487. PubMedCrossRef
24.
Zurück zum Zitat Tzivion, G., Dobson, M., & Ramakrishnan, G. (2011). FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochimica et Biophysica Acta, 1813(11), 1938–1945. PubMedCrossRef Tzivion, G., Dobson, M., & Ramakrishnan, G. (2011). FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochimica et Biophysica Acta, 1813(11), 1938–1945. PubMedCrossRef
25.
Zurück zum Zitat Zhang, B., Turdi, S., Li, Q., Lopez, F. L., Eason, A. R., Anversa, P., et al. (2010). Cardiac overexpression of insulin-like growth factor 1 attenuates chronic alcohol intake-induced myocardial contractile dysfunction but not hypertrophy: Roles of Akt, mTOR, GSK3beta, and PTEN. Free Radical Biology & Medicine, 49(7), 1238–1253. CrossRef Zhang, B., Turdi, S., Li, Q., Lopez, F. L., Eason, A. R., Anversa, P., et al. (2010). Cardiac overexpression of insulin-like growth factor 1 attenuates chronic alcohol intake-induced myocardial contractile dysfunction but not hypertrophy: Roles of Akt, mTOR, GSK3beta, and PTEN. Free Radical Biology & Medicine, 49(7), 1238–1253. CrossRef
26.
Zurück zum Zitat Mohaddes, G., Abdolalizadeh, J., Babri, S., & Hossienzadeh, F. (2017). Ghrelin ameliorates blood-brain barrier disruption during systemic hypoxia. Experimental Physiology, 102(3), 376–382. PubMedCrossRef Mohaddes, G., Abdolalizadeh, J., Babri, S., & Hossienzadeh, F. (2017). Ghrelin ameliorates blood-brain barrier disruption during systemic hypoxia. Experimental Physiology, 102(3), 376–382. PubMedCrossRef
27.
Zurück zum Zitat Shirpoor, A., Nemati, S., Ansari, M. H., & Ilkhanizadeh, B. (2015). The protective effect of vitamin E against prenatal and early postnatal ethanol treatment-induced heart abnormality in rats: A 3-month follow-up study. International Immunopharmacology, 26(1), 72–79. PubMedCrossRef Shirpoor, A., Nemati, S., Ansari, M. H., & Ilkhanizadeh, B. (2015). The protective effect of vitamin E against prenatal and early postnatal ethanol treatment-induced heart abnormality in rats: A 3-month follow-up study. International Immunopharmacology, 26(1), 72–79. PubMedCrossRef
28.
Zurück zum Zitat Huynh, K. (2014). Risk factors. Reducing alcohol intake improves heart health. Nature Reviews Cardiology, 11(9), 495. PubMedCrossRef Huynh, K. (2014). Risk factors. Reducing alcohol intake improves heart health. Nature Reviews Cardiology, 11(9), 495. PubMedCrossRef
29.
Zurück zum Zitat Lluís, M., Fernández-Solà, J., Castellví-Bel, S., Sacanella, E., Estruch, R., & Urbano-Márquez, A. (2011). Evaluation of myocyte proliferation in alcoholic cardiomyopathy: Telomerase enzyme activity (TERT) compared with Ki-67 expression. Alcohol and Alcoholism (Oxford, Oxfordshire), 46(5), 534–541. CrossRef Lluís, M., Fernández-Solà, J., Castellví-Bel, S., Sacanella, E., Estruch, R., & Urbano-Márquez, A. (2011). Evaluation of myocyte proliferation in alcoholic cardiomyopathy: Telomerase enzyme activity (TERT) compared with Ki-67 expression. Alcohol and Alcoholism (Oxford, Oxfordshire), 46(5), 534–541. CrossRef
30.
Zurück zum Zitat Shirpoor, A., Norouzi, L., Khadem-Ansari, M. H., Ilkhanizadeh, B., & Karimipour, M. (2014). The protective effect of vitamin E on morphological and biochemical alteration induced by pre and postnatal ethanol administration in the testis of male rat offspring: A three months follow-up study. Journal of Reproduction & Infertility, 15(3), 134–141. Shirpoor, A., Norouzi, L., Khadem-Ansari, M. H., Ilkhanizadeh, B., & Karimipour, M. (2014). The protective effect of vitamin E on morphological and biochemical alteration induced by pre and postnatal ethanol administration in the testis of male rat offspring: A three months follow-up study. Journal of Reproduction & Infertility, 15(3), 134–141.
31.
Zurück zum Zitat Lan, N., Yamashita, F., Halpert, A. G., Ellis, L., Yu, W. K., Viau, V., et al. (2006). Prenatal ethanol exposure alters the effects of gonadectomy on hypothalamic-pituitary-adrenal activity in male rats. Journal of Neuroendocrinology, 18(9), 672–684. PubMedCrossRef Lan, N., Yamashita, F., Halpert, A. G., Ellis, L., Yu, W. K., Viau, V., et al. (2006). Prenatal ethanol exposure alters the effects of gonadectomy on hypothalamic-pituitary-adrenal activity in male rats. Journal of Neuroendocrinology, 18(9), 672–684. PubMedCrossRef
32.
Zurück zum Zitat Weinberg, J., Kim, C. K., & Yu, W. (1995). Early handling can attenuate adverse effects of fetal ethanol exposure. Alcohol (Fayetteville, NY), 12(4), 317–327. CrossRef Weinberg, J., Kim, C. K., & Yu, W. (1995). Early handling can attenuate adverse effects of fetal ethanol exposure. Alcohol (Fayetteville, NY), 12(4), 317–327. CrossRef
33.
Zurück zum Zitat Lan, N., Vogl, A. W., & Weinberg, J. (2013). Prenatal ethanol exposure delays the onset of spermatogenesis in the rat. Alcoholism, Clinical and Experimental Research, 37(7), 1074–1081. PubMedPubMedCentralCrossRef Lan, N., Vogl, A. W., & Weinberg, J. (2013). Prenatal ethanol exposure delays the onset of spermatogenesis in the rat. Alcoholism, Clinical and Experimental Research, 37(7), 1074–1081. PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Fakoya, F. A., & Caxton-Martins, E. A. (2004). Morphological alterations in the seminiferous tubules of adult Wistar rats: The effects of prenatal ethanol exposure. Folia Morphologica, 63(2), 195–202. PubMed Fakoya, F. A., & Caxton-Martins, E. A. (2004). Morphological alterations in the seminiferous tubules of adult Wistar rats: The effects of prenatal ethanol exposure. Folia Morphologica, 63(2), 195–202. PubMed
35.
Zurück zum Zitat Lajiness, J. D., & Conway, S. J. (2012). The dynamic role of cardiac fibroblasts in development and disease. Journal of Cardiovascular Translational Research, 5(6), 739–748. PubMedPubMedCentralCrossRef Lajiness, J. D., & Conway, S. J. (2012). The dynamic role of cardiac fibroblasts in development and disease. Journal of Cardiovascular Translational Research, 5(6), 739–748. PubMedPubMedCentralCrossRef
36.
Zurück zum Zitat Bao, M. W., Cai, Z., Zhang, X. J., Li, L., Liu, X., Wan, N., et al. (2015). Dickkopf-3 protects against cardiac dysfunction and ventricular remodelling following myocardial infarction. Basic Research in Cardiology, 110(3), 25. PubMedCrossRef Bao, M. W., Cai, Z., Zhang, X. J., Li, L., Liu, X., Wan, N., et al. (2015). Dickkopf-3 protects against cardiac dysfunction and ventricular remodelling following myocardial infarction. Basic Research in Cardiology, 110(3), 25. PubMedCrossRef
37.
Zurück zum Zitat Li, H., Cai, H., Deng, J., Tu, X., Sun, Y., Huang, Z., et al. (2018). TGF-β-mediated upregulation of Sox9 in fibroblast promotes renal fibrosis. Biochimica et Biophysica acta Molecular Basis of Disease, 1864(2), 520–532. PubMedCrossRef Li, H., Cai, H., Deng, J., Tu, X., Sun, Y., Huang, Z., et al. (2018). TGF-β-mediated upregulation of Sox9 in fibroblast promotes renal fibrosis. Biochimica et Biophysica acta Molecular Basis of Disease, 1864(2), 520–532. PubMedCrossRef
38.
Zurück zum Zitat Higgins, S. P., Tang, Y., Higgins, C. E., Mian, B., Zhang, W., Czekay, R. P., et al. (2018). TGF-β1/p53 signaling in renal fibrogenesis. Cellular Signalling, 43, 1–10. PubMedCrossRef Higgins, S. P., Tang, Y., Higgins, C. E., Mian, B., Zhang, W., Czekay, R. P., et al. (2018). TGF-β1/p53 signaling in renal fibrogenesis. Cellular Signalling, 43, 1–10. PubMedCrossRef
39.
Zurück zum Zitat Xiao, J., Sheng, X., Zhang, X., Guo, M., & Ji, X. (2016). Curcumin protects against myocardial infarction-induced cardiac fibrosis via SIRT1 activation in vivo and in vitro. Drug Design, Development and Therapy, 10, 1267–1277. PubMedPubMedCentral Xiao, J., Sheng, X., Zhang, X., Guo, M., & Ji, X. (2016). Curcumin protects against myocardial infarction-induced cardiac fibrosis via SIRT1 activation in vivo and in vitro. Drug Design, Development and Therapy, 10, 1267–1277. PubMedPubMedCentral
40.
Zurück zum Zitat March, J. T., Golshirazi, G., Cernisova, V., Carr, H., Leong, Y., Lu-Nguyen, N., et al. (2018). Targeting TGFβ signaling to address fibrosis using antisense oligonucleotides. Biomedicines, 6(3), 74. PubMedCentralCrossRef March, J. T., Golshirazi, G., Cernisova, V., Carr, H., Leong, Y., Lu-Nguyen, N., et al. (2018). Targeting TGFβ signaling to address fibrosis using antisense oligonucleotides. Biomedicines, 6(3), 74. PubMedCentralCrossRef
41.
Zurück zum Zitat Michishita, E., Park, J. Y., Burneskis, J. M., Barrett, J. C., & Horikawa, I. (2005). Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Molecular Biology of the Cell, 16(10), 4623–4635. PubMedPubMedCentralCrossRef Michishita, E., Park, J. Y., Burneskis, J. M., Barrett, J. C., & Horikawa, I. (2005). Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Molecular Biology of the Cell, 16(10), 4623–4635. PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Liu, Z. H., Zhang, Y., Wang, X., Fan, X. F., Zhang, Y., Li, X., et al. (2019). SIRT1 activation attenuates cardiac fibrosis by endothelial-to-mesenchymal transition Biomedicine & pharmacotherapy. Biomedecine & Pharmacotherapie, 118, 109227. CrossRef Liu, Z. H., Zhang, Y., Wang, X., Fan, X. F., Zhang, Y., Li, X., et al. (2019). SIRT1 activation attenuates cardiac fibrosis by endothelial-to-mesenchymal transition Biomedicine & pharmacotherapy. Biomedecine & Pharmacotherapie, 118, 109227. CrossRef
43.
Zurück zum Zitat Asadi-Azarbaijani, B., Braber, S., van Duursen, M., Jahnukainen, K., Santos, R., & Oskam, I. (2019). Imatinib mesylate does not counteract ovarian tissue fibrosis in postnatal rat ovary. Reproductive Biology, 19(2), 133–138. PubMedCrossRef Asadi-Azarbaijani, B., Braber, S., van Duursen, M., Jahnukainen, K., Santos, R., & Oskam, I. (2019). Imatinib mesylate does not counteract ovarian tissue fibrosis in postnatal rat ovary. Reproductive Biology, 19(2), 133–138. PubMedCrossRef
44.
Zurück zum Zitat Lin, C. H., Lin, C. C., Ting, W. J., Pai, P. Y., Kuo, C. H., Ho, T. J., et al. (2014). Resveratrol enhanced FOXO3 phosphorylation via synergetic activation of SIRT1 and PI3K/Akt signaling to improve the effects of exercise in elderly rat hearts. Age (Dordrecht, Netherlands), 36(5), 9705. CrossRef Lin, C. H., Lin, C. C., Ting, W. J., Pai, P. Y., Kuo, C. H., Ho, T. J., et al. (2014). Resveratrol enhanced FOXO3 phosphorylation via synergetic activation of SIRT1 and PI3K/Akt signaling to improve the effects of exercise in elderly rat hearts. Age (Dordrecht, Netherlands), 36(5), 9705. CrossRef
45.
Zurück zum Zitat Ni, H. M., Du, K., You, M., & Ding, W. X. (2013). Critical role of FoxO3a in alcohol-induced autophagy and hepatotoxicity. The American Journal of Pathology, 183(6), 1815–1825. PubMedPubMedCentralCrossRef Ni, H. M., Du, K., You, M., & Ding, W. X. (2013). Critical role of FoxO3a in alcohol-induced autophagy and hepatotoxicity. The American Journal of Pathology, 183(6), 1815–1825. PubMedPubMedCentralCrossRef
46.
Zurück zum Zitat Lai, L., Yan, L., Gao, S., Hu, C. L., Ge, H., Davidow, A., et al. (2013). Type 5 adenylyl cyclase increases oxidative stress by transcriptional regulation of manganese superoxide dismutase via the SIRT1/FoxO3a pathway. Circulation, 127(16), 1692–1701. PubMedPubMedCentralCrossRef Lai, L., Yan, L., Gao, S., Hu, C. L., Ge, H., Davidow, A., et al. (2013). Type 5 adenylyl cyclase increases oxidative stress by transcriptional regulation of manganese superoxide dismutase via the SIRT1/FoxO3a pathway. Circulation, 127(16), 1692–1701. PubMedPubMedCentralCrossRef
47.
Zurück zum Zitat Kwak, H. B., Lee, Y., Kim, J. H., Van Remmen, H., Richardson, A. G., & Lawler, J. M. (2015). MnSOD overexpression reduces fibrosis and pro-apoptotic signaling in the aging mouse heart. The Journals of Gerontology Series A, Biological Sciences and Medical Sciences, 70(5), 533–544. PubMedCrossRef Kwak, H. B., Lee, Y., Kim, J. H., Van Remmen, H., Richardson, A. G., & Lawler, J. M. (2015). MnSOD overexpression reduces fibrosis and pro-apoptotic signaling in the aging mouse heart. The Journals of Gerontology Series A, Biological Sciences and Medical Sciences, 70(5), 533–544. PubMedCrossRef
48.
Zurück zum Zitat Li, K., Zhai, M., Jiang, L., Song, F., Zhang, B., Li, J., et al. (2019). Tetrahydrocurcumin ameliorates diabetic cardiomyopathy by attenuating high glucose-induced oxidative stress and fibrosis via activating the SIRT1 pathway. Oxidative Medicine and Cellular Longevity, 2019, 6746907. PubMedPubMedCentral Li, K., Zhai, M., Jiang, L., Song, F., Zhang, B., Li, J., et al. (2019). Tetrahydrocurcumin ameliorates diabetic cardiomyopathy by attenuating high glucose-induced oxidative stress and fibrosis via activating the SIRT1 pathway. Oxidative Medicine and Cellular Longevity, 2019, 6746907. PubMedPubMedCentral
49.
Zurück zum Zitat Zhou, L., Li, P., Zhang, M., Han, B., Chu, C., Su, X., et al. (2020). Carbon black nanoparticles induce pulmonary fibrosis through NLRP3 inflammasome pathway modulated by miR-96 targeted FOXO3a. Chemosphere, 241, 125075. PubMedCrossRef Zhou, L., Li, P., Zhang, M., Han, B., Chu, C., Su, X., et al. (2020). Carbon black nanoparticles induce pulmonary fibrosis through NLRP3 inflammasome pathway modulated by miR-96 targeted FOXO3a. Chemosphere, 241, 125075. PubMedCrossRef
50.
Zurück zum Zitat Ni, Y., Deng, J., Liu, X., Li, Q., Zhang, J., Bai, H., et al. (2021). Echinacoside reverses myocardial remodeling and improves heart function via regulating SIRT1/FOXO3a/MnSOD axis in HF rats induced by isoproterenol. Journal of Cellular and Molecular Medicine, 25(1), 203–216. PubMedCrossRef Ni, Y., Deng, J., Liu, X., Li, Q., Zhang, J., Bai, H., et al. (2021). Echinacoside reverses myocardial remodeling and improves heart function via regulating SIRT1/FOXO3a/MnSOD axis in HF rats induced by isoproterenol. Journal of Cellular and Molecular Medicine, 25(1), 203–216. PubMedCrossRef
Metadaten
Titel
Maternal Ethanol Exposure-Induced Cardiac Fibrosis is Associated with Changes in TGF-β and SIRT1/FOXO3a Signaling in Male Rat Offspring: A Three-Month Follow-up Study
verfasst von
Alireza Shirpoor
Roya Naderi
Publikationsdatum
28.07.2022
Verlag
Springer US
Erschienen in
Cardiovascular Toxicology / Ausgabe 9/2022
Print ISSN: 1530-7905
Elektronische ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-022-09761-7

Weitere Artikel der Ausgabe 9/2022

Cardiovascular Toxicology 9/2022 Zur Ausgabe