Oxidative Stress in Maternal and Offspring Kidney Disease and Hypertension: A Life-Course Perspective
Abstract
:1. Introduction
2. Maternal–Fetal Interface and Oxidative Stress
2.1. Oxidative Stress in Pregnancy
2.2. Maternal Kidney Disease and Hypertension
2.3. Oxidative Stress and Human Kidney Development: A Missing Link?
3. Animal Evidence for Oxidative Stress-Related Kidney Programming
3.1. Maternal Insults
3.2. Oxidative Stress Programming Mechanisms
4. Antioxidants as a Strategy for Prevention and Treatment
4.1. Vitamins
4.2. Polyphenols
4.3. Amino Acids
4.4. Melatonin
4.5. Synthetic Antioxidants
4.6. Nitric Oxide-Targeted Therapies
4.7. Others
5. Research Gaps and Future Directions
6. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Barker, D.J.; Eriksson, J.G.; Forsen, T.; Osmond, C. Fetal origins of adult disease: Strength of effects and biological basis. Int. J. Epidemiol. 2002, 31, 1235–1239. [Google Scholar] [PubMed]
- Picó, C.; Reis, F.; Egas, C.; Mathias, P.; Matafome, P. Lactation as a programming window for metabolic syndrome. Eur. J. Clin. Investig. 2021, 51, e13482. [Google Scholar]
- Padmanabhan, V.; Cardoso, R.C.; Puttabyatappa, M. Developmental Programming, a Pathway to Disease. Endocrinology 2016, 157, 1328–1340. [Google Scholar]
- Fleming, T.P.; Velazquez, M.A.; Eckert, J.J. Embryos, DOHaD and David Barker. J. Dev. Orig. Health Dis. 2015, 6, 377–383. [Google Scholar] [PubMed]
- Wagner, C.; Carmeli, C.; Jackisch, J.; Kivimäki, M.; van der Linden, B.W.A.; Cullati, S.; Chiolero, A. Life course epidemiology and public health. Lancet Public. Health 2024, 9, e261–e269. [Google Scholar]
- Nüsken, E.; Dötsch, J.; Weber, L.T.; Nüsken, K.D. Developmental Programming of Renal Function and Re-Programming Approaches. Front. Pediatr. 2018, 6, 36. [Google Scholar]
- Paauw, N.D.; Van Rijn, B.B.; Lely, A.T.; Joles, J.A. Pregnancy as a critical window for blood pressure regulation in mother and child: Programming and reprogramming. Acta Physiol. 2016, 219, 241–259. [Google Scholar]
- Tain, Y.L.; Hsu, C.N. Oxidative Stress-Induced Hypertension of Developmental Origins: Preventive Aspects of Antioxidant Therapy. Antioxidants 2022, 11, 511. [Google Scholar] [CrossRef]
- Rodríguez-Rodríguez, P.; Ramiro-Cortijo, D.; Reyes-Hernández, C.G.; López de Pablo, A.L.; González, M.C.; Arribas, S.M. Implication of Oxidative Stress in Fetal Programming of Cardiovascular Disease. Front. Physiol. 2018, 9, 602. [Google Scholar]
- Tain, Y.L.; Hsu, C.N. Metabolic Syndrome Programming and Reprogramming: Mechanistic Aspects of Oxidative Stress. Antioxidants 2022, 11, 2108. [Google Scholar] [CrossRef]
- Thompson, L.P.; Al-Hasan, Y. Impact of oxidative stress in fetal programming. J. Pregnancy 2012, 2012, 582748. [Google Scholar] [CrossRef] [PubMed]
- Hussain, T.; Murtaza, G.; Metwally, E.; Kalhoro, D.H.; Kalhoro, M.S.; Rahu, B.A.; Sahito, R.G.A.; Yin, Y.; Yang, H.; Chughtai, M.I.; et al. The Role of Oxidative Stress and Antioxidant Balance in Pregnancy. Mediat. Inflamm. 2021, 2021, 9962860. [Google Scholar] [CrossRef]
- Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol. 2015, 4, 180–183. [Google Scholar] [CrossRef] [PubMed]
- GBD 2017 Risk Factor Collaborators. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990–2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet 2018, 392, 1923–1994. [Google Scholar]
- Reynolds, M.L.; Herrera, C.A. Chronic Kidney Disease and Pregnancy. Adv. Chronic Kidney Dis. 2020, 27, 461–468. [Google Scholar] [CrossRef]
- Agrawal, A.; Wenger, N.K. Hypertension During Pregnancy. Curr. Hypertens. Rep. 2020, 22, 64. [Google Scholar] [CrossRef]
- Evans, R.G.; Bie, P. Role of the kidney in the pathogenesis of hypertension: Time for a neo-Guytonian paradigm or a paradigm shift? Am. J. Physiol. Regul. Integr. Comp. Physiol. 2016, 310, R217–R229. [Google Scholar] [CrossRef]
- Luyckx, V.A.; Bertram, J.F.; Brenner, B.M.; Fall, C.; Hoy, W.E.; Ozanne, S.E.; Vikse, B.E. Effect of fetal and child health on kidney development and long-term risk of hypertension and kidney disease. Lancet 2013, 382, 273–283. [Google Scholar] [CrossRef]
- Tain, Y.L. Advocacy for DOHaD research optimizing child kidney health. Pediatr. Neonatol. 2025, 66, S18–S22. [Google Scholar] [CrossRef]
- Luyckx, V.A.; Chevalier, R.L. Impact of early life development on later onset chronic kidney disease and hypertension and the role of evolutionary trade-offs. Exp. Physiol. 2022, 107, 410–414. [Google Scholar] [CrossRef]
- Al Khalaf, S.; Bodunde, E.; Maher, G.M.; O’Reilly, É.J.; McCarthy, F.P.; O’Shaughnessy, M.M.; O’Neill, S.M.; Khashan, A.S. Chronic kidney disease and adverse pregnancy outcomes: A systematic review and meta-analysis. Am. J. Obstet. Gynecol. 2022, 226, 656–670.e32. [Google Scholar] [PubMed]
- Grzeszczak, K.; Łanocha-Arendarczyk, N.; Malinowski, W.; Ziętek, P.; Kosik-Bogacka, D. Oxidative Stress in Pregnancy. Biomolecules 2023, 13, 1768. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, A.; Khoo, M.I.; Ismail, E.H.E.; Hussain, N.H.N.; Zin, A.A.M.; Noordin, L.; Abdullah, S.; Mahdy, Z.A.; Lah, N.A.Z.N. Oxidative stress biomarkers in pregnancy: A systematic review. Reprod. Biol. Endocrinol. 2024, 22, 93. [Google Scholar] [CrossRef]
- Hsu, C.N.; Tain, Y.L. Developmental Origins of Kidney Disease: Why Oxidative Stress Matters? Antioxidants 2020, 10, 33. [Google Scholar] [CrossRef]
- Kett, M.M.; Denton, K.M. Renal programming: Cause for concern? Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300, R791–R803. [Google Scholar] [CrossRef]
- Shkolnik, K.; Tadmor, A.; Ben-Dor, S.; Nevo, N.; Galiani, D.; Dekel, N. Reactive oxygen species are indispensable in ovulation. Proc. Natl. Acad. Sci. USA 2011, 108, 1462–1467. [Google Scholar] [CrossRef]
- Guérin, P.; El Mouatassim, S.; Ménézo, Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 2001, 7, 175–189. [Google Scholar] [CrossRef]
- Myatt, L. Review: Reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 2010, 31, S66–S69. [Google Scholar] [CrossRef]
- Dennery, P.A. Oxidative stress in development: Nature or nurture? Free Radic. Biol. Med. 2010, 49, 1147–1151. [Google Scholar] [CrossRef]
- Carter, A.M. Placental oxygen consumption. Part, I. In vivo studies—A review. Placenta 2000, 21, S31–S37. [Google Scholar] [CrossRef]
- Afrose, D.; Johansen, M.D.; Nikolic, V.; Karadzov Orlic, N.; Mikovic, Z.; Stefanovic, M.; Cakic, Z.; Hansbro, P.M.; McClements, L. Evaluating oxidative stress targeting treatments in in vitro models of placental stress relevant to preeclampsia. Front. Cell Dev. Biol. 2025, 13, 1539496. [Google Scholar]
- Saucedo, R.; Ortega-Camarillo, C.; Ferreira-Hermosillo, A.; Díaz-Velázquez, M.F.; Meixueiro-Calderón, C.; Valencia-Ortega, J. Role of Oxidative Stress and Inflammation in Gestational Diabetes Mellitus. Antioxidants 2023, 12, 1812. [Google Scholar] [CrossRef]
- Zhang, C.X.W.; Candia, A.A.; Sferruzzi-Perri, A.N. Placental inflammation, oxidative stress, and fetal outcomes in maternal obesity. Trends Endocrinol. Metab. 2024, 35, 638–647. [Google Scholar]
- Aouache, R.; Biquard, L.; Vaiman, D.; Miralles, F. Oxidative stress in preeclampsia and placental diseases. Int. J. Mol. Sci. 2018, 19, 1496. [Google Scholar] [CrossRef]
- Joo, E.H.; Kim, Y.R.; Kim, N.; Jung, J.E.; Han, S.H.; Cho, H.Y. Effect of Endogenic and Exogenic Oxidative Stress Triggers on Adverse Pregnancy Outcomes: Preeclampsia, Fetal Growth Restriction, Gestational Diabetes Mellitus and Preterm Birth. Int. J. Mol. Sci. 2021, 22, 10122. [Google Scholar] [CrossRef]
- Zullino, S.; Buzzella, F.; Simoncini, T. Nitric oxide and the biology of pregnancy. Vascul. Pharmacol. 2018, 110, 71–74. [Google Scholar]
- Krause, B.J. Novel insights for the role of nitric oxide in placental vascular function during and beyond pregnancy. J. Cell Physiol. 2021, 236, 7984–7999. [Google Scholar]
- Huang, L.T.; Hsieh, C.S.; Chang, K.A.; Tain, Y.L. Roles of nitric oxide and asymmetric dimethylarginine in pregnancy and fetal programming. Int. J. Mol. Sci. 2012, 13, 14606–14622. [Google Scholar] [CrossRef]
- Hsu, C.N.; Tain, Y.L. Impact of Arginine Nutrition and Metabolism during Pregnancy on Offspring Outcomes. Nutrients 2019, 11, 1452. [Google Scholar] [CrossRef]
- Radi, R. Oxygen radicals, nitric oxide, and peroxynitrite: Redox pathways in molecular medicine. Proc. Natl. Acad. Sci. USA 2018, 115, 5839–5848. [Google Scholar]
- Piacenza, L.; Zeida, A.; Trujillo, M.; Radi, R. The superoxide radical switch in the biology of nitric oxide and peroxynitrite. Physiol. Rev. 2022, 102, 1881–1906. [Google Scholar]
- Baylis, C. Nitric oxide synthase derangements and hypertension in kidney disease. Curr. Opin. Nephrol. Hypertens. 2012, 21, 1–6. [Google Scholar]
- Wilcox, C.S. Oxidative stress and nitric oxide deficiency in the kidney: A critical link to hypertension? Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289, R913–R935. [Google Scholar]
- Fickling, S.A.; Williams, D.; Vallance, P.; Nussey, S.S.; Whitley, G.S. Plasma of endogenous inhibitor of nitric oxide synthesis in normal pregnancy and pre-eclampsia. Lancet 1993, 342, 242–243. [Google Scholar]
- Holden, D.P.; Fickling, S.A.; Whitley, G.S.; Nussey, S.S. Plasma concentrations of asymmetric dimethylarginine, a natural inhibitor of nitric oxide synthase, in normal pregnancy and preeclampsia. Am. J. Obstet. Gynecol. 1998, 178, 551–556. [Google Scholar]
- Vida, G.; Sulyok, E.; Ertl, T.; Martens-Lobenhoffer, J.; Bode-Böger, S.M. Birth by cesarean section is associated with elevated neonatal plasma levels of dimethylarginines. Pediatr. Int. 2012, 54, 476–479. [Google Scholar]
- Akturk, M.; Altinova, A.; Mert, I.; Dincel, A.; Sargin, A.; Buyukkagnici, U.; Arslan, M.; Danisman, N. Asymmetric dimethylarginine concentrations are elevated in women with gestational diabetes. Endocrine 2010, 38, 134–141. [Google Scholar]
- Németh, B.; Murányi, E.; Hegyi, P.; Mátrai, P.; Szakács, Z.; Varjú, P.; Hamvas, S.; Tinusz, B.; Budán, F.; Czimmer, J.; et al. Asymmetric dimethylarginine levels in preeclampsia—Systematic review and meta-analysis. Placenta 2018, 69, 57–63. [Google Scholar]
- Rijvers, C.A.; Marzano, S.; Winkens, B.; Bakker, J.A.; Kroon, A.A.; Spaanderman, M.E.; Peeters, L.L. Early-pregnancy asymmetric dimethylarginine (ADMA) levels in women prone to develop recurrent hypertension. Pregnancy Hypertens. 2013, 3, 118–123. [Google Scholar]
- Kishi, S.; Nagasu, H.; Kidokoro, K.; Kashihara, N. Oxidative stress and the role of redox signalling in chronic kidney disease. Nat. Rev. Nephrol. 2024, 20, 101–119. [Google Scholar]
- Daenen, K.; Andries, A.; Mekahli, D.; Van Schepdael, A.; Jouret, F.; Bammens, B. Oxidative stress in chronic kidney disease. Pediatr. Nephrol. 2019, 34, 975–991. [Google Scholar] [CrossRef] [PubMed]
- Espinoza, J.; Vidaeff, A.; Pettker, C.M.; Simhan, H. Gestational Hypertension and Preeclampsia: ACOG Practice Bulletin, Number 222. Obstet. Gynecol. 2020, 135, e237–e260. [Google Scholar]
- Cífková, R. Hypertension in Pregnancy: A Diagnostic and Therapeutic Overview. High. Blood Press. Cardiovasc. Prev. 2023, 30, 289–303. [Google Scholar] [CrossRef] [PubMed]
- Barbosa, P.O.; Tanus-Santos, J.E.; Cavalli, R.C.; Bengtsson, T.; Montenegro, M.F.; Sandrim, V.C. The Nitrate-Nitrite-Nitric Oxide Pathway: Potential Role in Mitigating Oxidative Stress in Hypertensive Disorders of Pregnancy. Nutrients 2024, 16, 1475. [Google Scholar] [CrossRef]
- Chiarello, D.I.; Abad, C.; Rojas, D.; Toledo, F.; Vázquez, C.M.; Mate, A.; Sobrevia, L.; Marín, R. Oxidative stress: Normal pregnancy versus preeclampsia. Biochim. Biophys. Acta Mol. Basis Dis. 2020, 1866, 165354. [Google Scholar] [CrossRef]
- Taysi, S.; Tascan, A.S.; Ugur, M.G.; Demir, M. Radicals, Oxidative/Nitrosative Stress and Preeclampsia. Mini. Rev. Med. Chem. 2019, 19, 178–193. [Google Scholar] [CrossRef]
- Hinchliffe, S.A.; Sargent, P.H.; Howard, C.V.; Chan, Y.F.; van Velzen, D. Human intrauterine renal growth expressed in absolute number of glomeruli assessed by the disector method and Cavalieri principle. Lab. Investig. 1991, 64, 777–784. [Google Scholar]
- Shah, M.M.; Sampogna, R.V.; Sakurai, H.; Bush, K.T.; Nigam, S.K. Branching morphogenesis and kidney disease. Development 2004, 131, 1449–1462. [Google Scholar] [CrossRef]
- Luyckx, V.A.; Brenner, B.M. The clinical importance of nephron mass. J. Am. Soc. Nephrol. 2010, 21, 898–910. [Google Scholar] [CrossRef]
- Bertram, J.F.; Douglas-Denton, R.N.; Diouf, B.; Hughson, M.; Hoy, W. Human nephron number: Implications for health and disease. Pediatr. Nephrol. 2011, 26, 1529–1533. [Google Scholar] [CrossRef]
- Rosenbaum, D.M.; Korngold, E.; Teele, R.L. Sonographic assessment of renal length in normal children. Am. J. Roentgenol. 1984, 142, 467–469. [Google Scholar] [CrossRef] [PubMed]
- Filler, G.; Lopes, L.; Awuku, M. The importance of accurately assessing renal function in the neonate and infant. Adv. Clin. Chem. 2015, 71, 141–156. [Google Scholar] [PubMed]
- Liu, L.; Barajas, L. The rat renal nerves during development. Anat. Embryol. 1993, 188, 345–361. [Google Scholar] [CrossRef] [PubMed]
- Nenov, V.D.; Taal, M.W.; Sakharova, O.V.; Brenner, B.M. Multi-hit nature of chronic renal disease. Curr. Opin. Nephrol. Hypertens. 2000, 9, 85–97. [Google Scholar]
- Tain, Y.L.; Hsieh, C.S.; Lin, I.C.; Chen, C.C.; Sheen, J.M.; Huang, L.T. Effects of maternal L-citrulline supplementation on renal function and blood pressure in offspring exposed to maternal caloric restriction: The impact of nitric oxide pathway. Nitric Oxide 2010, 23, 34–41. [Google Scholar] [CrossRef]
- Tain, Y.L.; Huang, L.T.; Hsu, C.N.; Lee, C.T. Melatonin therapy prevents programmed hypertension and nitric oxide deficiency in offspring exposed to maternal caloric restriction. Oxid. Med. Cell Longev. 2014, 2014, 283180. [Google Scholar] [CrossRef]
- Cambonie, G.; Comte, B.; Yzydorczyk, C.; Ntimbane, T.; Germain, N.; Lê, N.L.; Pladys, P.; Gauthier, C.; Lahaie, I.; Abran, D.; et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292, R1236–R1245. [Google Scholar]
- Tain, Y.L.; Lee, W.C.; Wu, K.L.H.; Leu, S.; Chan, J.Y.H. Targeting arachidonic acid pathway to prevent programmed hypertension in maternal fructose-fed male adult rat offspring. J. Nutr. Biochem. 2016, 38, 86–92. [Google Scholar] [CrossRef]
- Tain, Y.L.; Chan, J.Y.H.; Lee, C.T.; Hsu, C.N. Maternal Melatonin Therapy Attenuates Methyl-Donor Diet-Induced Programmed Hypertension in Male Adult Rat Offspring. Nutrients 2018, 10, 1407. [Google Scholar] [CrossRef]
- Chang, Y.H.; Chen, W.H.; Su, C.H.; Yu, H.R.; Tain, Y.L.; Huang, L.T.; Sheen, J.M. Maternal Iron Deficiency Programs Rat Offspring Hypertension in Relation to Renin-Angiotensin System and Oxidative Stress. Int. J. Mol. Sci. 2022, 23, 8294. [Google Scholar] [CrossRef]
- Tain, Y.L.; Lee, W.C.; Wu, K.L.H.; Leu, S.; Chan, J.Y.H. Resveratrol Prevents the Development of Hypertension Programmed by Maternal Plus Post-Weaning High-Fructose Consumption through Modulation of Oxidative Stress, Nutrient-Sensing Signals, and Gut Microbiota. Mol. Nutr. Food Res. 2018, 30, e1800066. [Google Scholar]
- Do Nascimento, L.C.P.; Neto, J.P.R.C.; de Andrade Braga, V.; Lagranha, C.J.; de Brito Alves, J.L. Maternal exposure to high-fat and high-cholesterol diet induces arterial hypertension and oxidative stress along the gut-kidney axis in rat offspring. Life Sci. 2020, 261, 118367. [Google Scholar] [CrossRef]
- Tain, Y.L.; Lin, Y.J.; Sheen, J.M.; Yu, H.R.; Tiao, M.M.; Chen, C.C.; Tsai, C.C.; Huang, L.T.; Hsu, C.N. High Fat Diets Sex-Specifically Affect the Renal Transcriptome and Program Obesity, Kidney Injury, and Hypertension in the Offspring. Nutrients 2017, 9, 357. [Google Scholar] [CrossRef] [PubMed]
- do Nascimento, L.C.P.; de Souza, E.L.; de Luna Freire, M.O.; de Andrade Braga, V.; de Albuqeurque, T.M.R.; Lagranha, C.J.; de Brito Alves, J.L. Limosilactobacillus fermentum prevent gut-kidney oxidative damage and the rise in blood pressure in male rat offspring exposed to a maternal high-fat diet. J. Dev. Orig. Health Dis. 2022, 19, 1–8. [Google Scholar]
- Nguyen, L.T.; Mak, C.H.; Chen, H.; Zaky, A.A.; Wong, M.G.; Pollock, C.A.; Saad, S. SIRT1 Attenuates Kidney Disorders in Male Offspring Due to Maternal High-Fat Diet. Nutrients 2019, 11, 146. [Google Scholar] [CrossRef]
- Ojeda, N.B.; Hennington, B.S.; Williamson, D.T.; Hill, M.L.; Betson, N.E.; Sartori-Valinotti, J.C.; Reckelhoff, J.F.; Royals, T.P.; Alexander, B.T. Oxidative stress contributes to sex differences in blood pressure in adult growth-restricted offspring. Hypertension 2012, 60, 114–122. [Google Scholar]
- Tain, Y.L.; Lee, W.C.; Hsu, C.N.; Lee, W.C.; Huang, L.T.; Lee, C.T.; Lin, C.Y. Asymmetric dimethylarginine is associated with developmental programming of adult kidney disease and hypertension in offspring of streptozotocin-treated mothers. PLoS ONE 2013, 8, e55420. [Google Scholar]
- Martínez Gascón, L.E.; Ortiz, M.C.; Galindo, M.; Sanchez, J.M.; Sancho-Rodriguez, N.; Albaladejo Otón, M.D.; Rodriguez Mulero, M.D.; Rodriguez, F. Role of heme oxygenase in the regulation of the renal hemodynamics in a model of sex dependent programmed hypertension by maternal diabetes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2022, 322, R181–R191. [Google Scholar]
- Tain, Y.L.; Lee, C.T.; Chan, J.Y.; Hsu, C.N. Maternal melatonin or N-acetylcysteine therapy regulates hydrogen sulfide-generating pathway and renal transcriptome to prevent prenatal N(G)-Nitro-L-arginine methyl ester (L-NAME)-induced fetal programming of hypertension in adult male offspring. Am. J. Obstet. Gynecol. 2016, 215, 636. [Google Scholar]
- Tain, Y.L.; Hsu, C.N.; Lee, C.T.; Lin, Y.J.; Tsai, C.C. N-Acetylcysteine prevents programmed hypertension in male rat offspring born to suramin-treated mothers. Biol. Reprod. 2016, 95, 8. [Google Scholar] [CrossRef]
- Hsu, C.N.; Yang, H.W.; Hou, C.Y.; Chang-Chien, G.P.; Lin, S.; Tain, Y.L. Maternal Adenine-Induced Chronic Kidney Disease Programs Hypertension in Adult Male Rat Offspring: Implications of Nitric Oxide and Gut Microbiome Derived Metabolites. Int. J. Mol. Sci. 2020, 21, 7237. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.N.; Hou, C.Y.; Chang-Chien, G.P.; Lin, S.; Yang, H.W.; Tain, Y.L. Perinatal Resveratrol Therapy Prevents Hypertension Programmed by Maternal Chronic Kidney Disease in Adult Male Offspring: Implications of the Gut Microbiome and Their Metabolites. Biomedicines 2020, 8, 567. [Google Scholar] [CrossRef]
- Svitok, P.; Okuliarova, M.; Varga, I.; Zeman, M. Renal impairment induced by prenatal exposure to angiotensin II in male rat offspring. Exp. Biol. Med. (Maywood) 2019, 244, 923–931. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.N.; Hou, C.Y.; Chang-Chien, G.P.; Lin, S.; Chan, J.Y.H.; Lee, C.T.; Tain, Y.L. Maternal resveratrol therapy protected adult rat offspring against hypertension programmed by combined exposures to asymmetric dimethylarginine and trimethylamine-N-oxide. J. Nutr. Biochem. 2021, 93, 108630. [Google Scholar] [CrossRef] [PubMed]
- Vieira, L.D.; Farias, J.S.; de Queiroz, D.B.; Cabral, E.V.; Lima-Filho, M.M.; Sant’Helena, B.R.M.; Aires, R.S.; Ribeiro, V.S.; SantosRocha, J.; Xavier, F.E.; et al. Oxidative stress induced by prenatal LPS leads to endothelial dysfunction and renal haemodynamic changes through angiotensin II/NADPH oxidase pathway: Prevention by early treatment with α-tocopherol. Biochim. Biophys. Acta Mol. Basis Dis. 2018, 1864, 3577–3587. [Google Scholar] [CrossRef]
- Cao, N.; Lan, C.; Chen, C.; Xu, Z.; Luo, H.; Zheng, S.; Gong, X.; Ren, H.; Li, Z.; Qu, S.; et al. Prenatal Lipopolysaccharides Exposure Induces Transgenerational Inheritance of Hypertension. Circulation. 2022, 146, 1082–1095. [Google Scholar] [CrossRef]
- Jeje, S.O.; Akindele, O.O.; Ushie, G.; Rajil, Y. Changes in kidney function and oxidative stress biomarkers in offspring from dams treated with dexamethasone during lactation in Wistar rats. Afr. J. Med. Med. Sci. 2016, 45, 237–242. [Google Scholar]
- Tain, Y.L.; Sheen, J.M.; Chen, C.C.; Yu, H.R.; Tiao, M.M.; Kuo, H.C.; Huang, L.T. Maternal citrulline supplementation prevents prenatal dexamethasone-induced programmed hypertension. Free Radic. Res. 2014, 48, 580–586. [Google Scholar] [CrossRef]
- Gwathmey, T.M.; Shaltout, H.A.; Rose, J.C.; Diz, D.I.; Chappell, M.C. Glucocorticoid-induced fetal programming alters the functional complement of angiotensin receptor subtypes within the kidney. Hypertension 2011, 57, 620–626. [Google Scholar]
- Sukjamnong, S.; Chan, Y.L.; Zakarya, R.; Nguyen, L.T.; Anwer, A.G.; Zaky, A.A.; Santiyanont, R.; Oliver, B.G.; Goldys, E.; Pollock, C.A.; et al. MitoQ supplementation prevent long-term impact of maternal smoking on renal development, oxidative stress and mitochondrial density in male mice offspring. Sci. Rep. 2018, 8, 6631. [Google Scholar]
- Zhu, Y.P.; Chen, L.; Wang, X.J.; Jiang, Q.H.; Bei, X.Y.; Sun, W.L.; Xia, S.J.; Jiang, J.T. Maternal exposure to di-n-butyl phthalate (DBP) induces renal fibrosis in adult rat offspring. Oncotarget 2017, 8, 31101–31111. [Google Scholar] [PubMed]
- Hsu, C.N.; Lin, Y.J.; Tain, Y.L. Maternal exposure to bisphenol A combined with high-fat diet-induced programmed hypertension in adult male rat offspring: Effects of resveratrol. Int. J. Mol. Sci. 2019, 20, 4382. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.N.; Lin, Y.J.; Lu, P.C.; Tain, Y.L. Maternal resveratrol therapy protects male rat offspring against programmed hypertension induced by TCDD and dexamethasone exposures: Is it relevant to aryl hydrocarbon receptor? Int. J. Mol. Sci. 2018, 19, 2459. [Google Scholar] [CrossRef] [PubMed]
- Kuczeriszka, M.; Wąsowicz, K. Animal models of hypertension: The status of nitric oxide and oxidative stress and the role of the renal medulla. Nitric Oxide 2022, 125–126, 40–46. [Google Scholar] [CrossRef]
- Rubera, I.; Hummler, E.; Beermann, F. Transgenic mice and their impact on kidney research. Pflugers. Arch. 2009, 458, 211–222. [Google Scholar]
- Perrone, S.; Laschi, E.; Buonocore, G. Biomarkers of oxidative stress in the fetus and in the newborn. Free Radic. Biol. Med. 2019, 142, 23–31. [Google Scholar]
- Pilger, A.; Rüdiger, H.W. 8-Hydroxy-2′-deoxyguanosine as a marker of oxidative DNA damage related to occupational and environmental exposures. Int. Arch. Occup. Environ. Health 2006, 80, 1–15. [Google Scholar] [CrossRef]
- Bianco-Miotto, T.; Craig, J.M.; Gasser, Y.P.; van Dijk, S.J.; Ozanne, S.E. Epigenetics and DOHaD: From basics to birth and beyond. J. Dev. Orig. Health Dis. 2017, 8, 513–519. [Google Scholar] [CrossRef]
- Bhat, A.V.; Hora, S.; Pal, A.; Jha, S.; Taneja, R. Stressing the (Epi) Genome: Dealing with Reactive Oxygen Species in Cancer. Antioxid. Redox Signal. 2018, 29, 1273–1292. [Google Scholar]
- Vasudevan, D.; Bovee, R.C.; Thomas, D.D. Nitric oxide, the new architect of epigenetic landscapes. Nitric Oxide 2016, 59, 54–62. [Google Scholar]
- Tain, Y.L.; Huang, L.T.; Chan, J.Y.; Lee, C.T. Transcriptome analysis in rat kidneys: Importance of genes involved in programmed hypertension. Int. J. Mol. Sci. 2015, 16, 4744–4758. [Google Scholar] [CrossRef] [PubMed]
- Berger, R.G.; Lunkenbein, S.; Ströhle, A.; Hahn, A. Antioxidants in food: Mere myth or magic medicine? Crit. Rev. Food Sci. Nutr. 2012, 52, 162–171. [Google Scholar] [CrossRef] [PubMed]
- Jun, M.; Venkataraman, V.; Razavian, M.; Cooper, B.; Zoungas, S.; Ninomiya, T.; Webster, A.C.; Perkovic, V. Antioxidants for chronic kidney disease. Cochrane Database Syst. Rev. 2012, 10, CD008176. [Google Scholar] [PubMed]
- Buonocore, G.; Groenendaal, F. Anti-oxidant strategies. Semin. Fetal Neonatal Med. 2007, 12, 287–295. [Google Scholar]
- National Academy of Sciences, Institute of Medicine. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids: A Report of the Panel on Dietary Antioxidants and Related Compounds, Subcommittees on Upper Reference Levels of Nutrients and on Interpretation and Use of Dietary Reference Intakes, and the Standing Committee on Scientific Evaluation of Dietary Reference Intakes, Food and Nutrition Board; Institute of Medicine, 17 National Academy Press: Washington, DC, USA, 2000. [Google Scholar]
- Rapa, S.F.; Di Iorio, B.R.; Campiglia, P.; Heidland, A.; Marzocco, S. Inflammation and Oxidative Stress in Chronic Kidney Disease-Potential Therapeutic Role of Minerals, Vitamins and Plant-Derived Metabolites. Int. J. Mol. Sci. 2019, 21, 263. [Google Scholar] [CrossRef]
- Said, H.M.; Nexo, E. Gastrointestinal Handling of Water-Soluble Vitamins. Compr. Physiol. 2018, 8, 1291–1311. [Google Scholar]
- Niki, E. Role of vitamin E as a lipid-soluble peroxyl radical scavenger: In vitro and in vivo evidence. Free Radic. Biol. Med. 2014, 66, 3–12. [Google Scholar]
- Franco Mdo, C.; Ponzio, B.F.; Gomes, G.N.; Gil, F.Z.; Tostes, R.; Carvalho, M.H.; Fortes, Z.B. Micronutrient prenatal supplementation prevents the development of hypertension and vascular endothelial damage induced by intrauterine malnutrition. Life Sci. 2009, 85, 327–333. [Google Scholar]
- Wang, J.; Yin, N.; Deng, Y.; Wei, Y.; Huang, Y.; Pu, X.; Li, L.; Zheng, Y.; Guo, J.; Yu, J.; et al. Ascorbic Acid Protects against Hypertension through Downregulation of ACE1 Gene Expression Mediated by Histone Deacetylation in Prenatal InflammationInduced Offspring. Sci. Rep. 2016, 6, 39469. [Google Scholar]
- Farias, J.S.; Santos, K.M.; Lima, N.K.S.; Cabral, E.V.; Aires, R.S.; Veras, A.C.; Paixão, A.D.; Vieira, L.D. Maternal endotoxemia induces renal collagen deposition in adult offspring: Role of NADPH oxidase/TGF-β1/MMP-2 signaling pathway. Arch. Biochem. Biophys. 2020, 684, 108306. [Google Scholar]
- Bjelakovic, G.; Nikolova, D.; Gluud, L.L.; Simonetti, R.G.; Gluud, C. Antioxidant supplements for prevention of mortality in healthy participants and patients with various diseases. Cochrane Database Syst. Rev. 2012, 3, CD007176. [Google Scholar]
- Azaïs-Braesco, V.; Pascal, G. Vitamin A in pregnancy: Requirements and safety limits. Am. J. Clin. Nutr. 2000, 71, 1325S–1333S. [Google Scholar] [CrossRef] [PubMed]
- Schwalfenberg, G.; Rodushkin, I.; Genuis, S.J. Heavy metal contamination of prenatal vitamins. Toxicol. Rep. 2018, 5, 390–395. [Google Scholar] [CrossRef] [PubMed]
- Durazzo, A.; Lucarini, M.; Souto, E.B.; Cicala, C.; Caiazzo, E.; Izzo, A.A.; Novellino, E.; Santini, A. Polyphenols: A concise over-view on the chemistry, occurrence, and human health. Phytother. Res. 2019, 33, 2221–2243. [Google Scholar] [CrossRef]
- Bao, H.; Peng, A. The Green Tea Polyphenol (-)-epigallocatechin-3-gallate and its beneficial roles in chronic kidney disease. J. Transl. Int. Med. 2016, 4, 99–103. [Google Scholar] [CrossRef]
- Guerreiro, Í.; Ferreira-Pêgo, C.; Carregosa, D.; Santos, C.N.; Menezes, R.; Fernandes, A.S.; Costa, J.G. Polyphenols and Their Metabolites in Renal Diseases: An Overview. Foods 2022, 11, 1060. [Google Scholar] [CrossRef]
- Nacka-Aleksić, M.; Pirković, A.; Vilotić, A.; Bojić-Trbojević, Ž.; Jovanović Krivokuća, M.; Giampieri, F.; Battino, M.; Dekanski, D. The Role of Dietary Polyphenols in Pregnancy and Pregnancy-Related Disorders. Nutrients 2022, 14, 5246. [Google Scholar] [CrossRef]
- Darby, J.R.T.; Mohd Dollah, M.H.B.; Regnault, T.R.H.; Williams, M.T.; Morrison, J.L. Systematic review: Impact of resveratrol exposure during pregnancy on maternal and fetal outcomes in animal models of human pregnancy complications-Are we ready for the clinic? Pharmacol. Res. 2019, 144, 264–278. [Google Scholar] [CrossRef]
- Zhou, J.; Ren, Y.; Yu, J.; Zeng, Y.; Ren, J.; Wu, Y.; Zhang, Q.; Xiao, X. The effect of maternal dietary polyphenol consumption on offspring metabolism. Crit. Rev. Food. Sci. Nutr. 2024, 19, 1–18. [Google Scholar] [CrossRef]
- Tain, Y.L.; Hsu, C.N. Maternal Polyphenols and Offspring Cardiovascular-Kidney-Metabolic Health. Nutrients 2024, 16, 3168. [Google Scholar] [CrossRef]
- Wu, Z.; Zhao, J.; Xu, H.; Lyv, Y.; Feng, X.; Fang, Y.; Xu, Y. Maternal quercetin administration during gestation and lactation decrease endoplasmic reticulum stress and related inflammation in the adult offspring of obese female rats. Eur. J. Nutr. 2014, 53, 1669–1683. [Google Scholar] [PubMed]
- Lamothe, J.; Khurana, S.; Tharmalingam, S.; Williamson, C.; Byrne, C.J.; Lees, S.J.; Khaper, N.; Kumar, A.; Tai, T.C. Oxidative Stress Mediates the Fetal Programming of Hypertension by Glucocorticoids. Antioxidants 2021, 10, 531. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.P.; Singh, R.; Verma, S.S.; Rai, V.; Kaschula, C.H.; Maiti, P.; Gupta, S.C. Health benefits of resveratrol: Evidence from 926 clinical studies. Med. Res. Rev. 2019, 39, 1851–1891. [Google Scholar] [CrossRef]
- Truong, V.L.; Jun, M.; Jeong, W.S. Role of resveratrol in regulation of cellular defense systems against oxidative stress. Biofactors 2018, 44, 36–49. [Google Scholar] [PubMed]
- Walle, T.; Hsieh, F.; DeLegge, M.H.; Oatis, J.E., Jr.; Walle, U.K. High absorption but very low bioavailability of oral resveratrol 957 in humans. Drug Metab. Dispos. 2004, 32, 1377–1382. [Google Scholar] [CrossRef]
- Filippou, C.; Tatakis, F.; Polyzos, D.; Manta, E.; Thomopoulos, C.; Nihoyannopoulos, P.; Tousoulis, D.; Tsioufis, K. Overview of salt restriction in the Dietary Approaches to Stop Hypertension (DASH) and the Mediterranean diet for blood pressure reduction. Rev. Cardiovasc. Med. 2022, 23, 36. [Google Scholar] [CrossRef]
- Chan, M.; Kelly, J.; Tapsell, L. Dietary Modeling of Foods for Advanced CKD Based on General Healthy Eating Guidelines: What Should Be on the Plate? Am. J. Kidney Dis. 2017, 69, 436–450. [Google Scholar]
- Gantenbein, K.V.; Kanaka-Gantenbein, C. Mediterranean Diet as an Antioxidant: The Impact on Metabolic Health and Overall Wellbeing. Nutrients 2021, 13, 1951. [Google Scholar] [CrossRef]
- Schwingshackl, L.; Morze, J.; Hoffmann, G. Mediterranean diet and health status: Active ingredients and pharmacological mechanisms. Br. J. Pharmacol. 2020, 177, 1241–1257. [Google Scholar] [CrossRef]
- Villarejo, A.B.; Ramírez-Sánchez, M.; Segarra, A.B.; Martínez-Cañamero, M.; Prieto, I. Influence of extra virgin olive oil on blood pressure and kidney angiotensinase activities in spontaneously hypertensive rats. Planta. Med. 2015, 81, 664–669. [Google Scholar] [CrossRef]
- Ali, S.S.; Ahsan, H.; Zia, M.K.; Siddiqui, T.; Khan, F.H. Understanding oxidants and antioxidants: Classical team with new players. J. Food Biochem. 2020, 44, e13145. [Google Scholar]
- Li, X.; Zheng, S.; Wu, G. Amino Acid Metabolism in the Kidneys: Nutritional and Physiological Significance. Adv. Exp. Med. Biol. 2020, 1265, 71–95. [Google Scholar]
- Tain, Y.L.; Hsu, C.N. Amino Acids during Pregnancy and Offspring Cardiovascular-Kidney-Metabolic Health. Nutrients 2024, 16, 1263. [Google Scholar] [CrossRef] [PubMed]
- Cynober, L.; Moinard, C.; De Bandt, J.P. The 2009 ESPEN Sir David Cuthbertson. Citrulline: A new major signaling molecule or just another player in the pharmaconutrition game? Clin. Nutr. 2010, 29, 545–551. [Google Scholar]
- Hsu, C.N.; Lin, I.C.; Yu, H.R.; Huang, L.T.; Tiao, M.M.; Tain, Y.L. Maternal Tryptophan Supplementation Protects Adult Rat Offspring against Hypertension Programmed by Maternal Chronic Kidney Disease: Implication of Tryptophan-Metabolizing Microbiome and Aryl Hydrocarbon Receptor. Int. J. Mol. Sci. 2020, 21, 4552. [Google Scholar] [CrossRef] [PubMed]
- Hsu, C.N.; Hou, C.Y.; Chang-Chien, G.P.; Lin, S.; Tain, Y.L. Dietary Supplementation with Cysteine during Pregnancy Rescues Maternal Chronic Kidney Disease-Induced Hypertension in Male Rat Offspring: The Impact of Hydrogen Sulfide and Microbiota-Derived Tryptophan Metabolites. Antioxidants 2022, 11, 483. [Google Scholar] [CrossRef]
- Thaeomor, A.; Teangphuck, P.; Chaisakul, J.; Seanthaweesuk, S.; Somparn, N.; Roysommuti, S. Perinatal Taurine Supplementation Prevents Metabolic and Cardiovascular Effects of Maternal Diabetes in Adult Rat Offspring. Adv. Exp. Med. Biol. 2017, 975, 295–305. [Google Scholar]
- Reiter, R.J.; Mayo, J.C.; Tan, D.X.; Sainz, R.M.; Alatorre-Jimenez, M.; Qin, L. Melatonin as an antioxidant: Under promises but over delivers. J. Pineal Res. 2016, 61, 253–278. [Google Scholar] [CrossRef]
- Hardeland, R.; Tan, D.X.; Reiter, R.J. Kynuramines, metabolites of melatonin and other indoles: The resurrection of an almost forgotten class of biogenic amines. J. Pineal Res. 2009, 47, 109–126. [Google Scholar]
- Meng, X.; Li, Y.; Li, S.; Zhou, Y.; Gan, R.Y.; Xu, D.P.; Li, H.B. Dietary Sources and Bioactivities of Melatonin. Nutrients 2017, 9, 367. [Google Scholar] [CrossRef]
- Tamura, H.; Nakamura, Y.; Terron, M.P.; Flores, L.J.; Manchester, L.C.; Tan, D.X.; Sugino, N.; Reiter, R.J. Melatonin and pregnancy in the human. Reprod. Toxicol. 2008, 25, 291–303. [Google Scholar] [PubMed]
- Reiter, R.J.; Tan, D.X.; Terron, M.P.; Flores, L.J.; Czarnocki, Z. Melatonin and its metabolites: New findings regarding their production and their radical scavenging actions. Acta Biochim. Pol. 2007, 54, 1–9. [Google Scholar] [PubMed]
- Tain, Y.L.; Hsu, C.N. Melatonin Use during Pregnancy and Lactation Complicated by Oxidative Stress: Focus on Offspring’s Cardiovascular-Kidney-Metabolic Health in Animal Models. Antioxidants 2024, 13, 226. [Google Scholar] [CrossRef] [PubMed]
- Aversa, S.; Pellegrino, S.; Barberi, I.; Reiter, R.J.; Gitto, E. Potential utility of melatonin as an antioxidant during pregnancy and in the perinatal period. J. Matern. Fetal Neonatal Med. 2012, 25, 207–221. [Google Scholar]
- Shenoy, P.; Etcheverry, A.; Ia, J.; Witmans, M.; Tablizo, M.A. Melatonin Use in Pediatrics: A Clinical Review on Indications, Multisystem Effects, and Toxicity. Children 2024, 11, 323. [Google Scholar] [CrossRef]
- Marseglia, L.; D’Angelo, G.; Manti, S.; Reiter, R.J.; Gitto, E. Potential utility of melatonin in preeclampsia, intrauterine fetal growth retardation, and perinatal asphyxia. Reprod. Sci. 2016, 23, 970–977. [Google Scholar]
- Chitimus, D.M.; Popescu, M.R.; Voiculescu, S.E.; Panaitescu, A.M.; Pavel, B.; Zagrean, L.; Zagrean, A.M. Melatonin’s Impact on Antioxidative and Anti-Inflammatory Reprogramming in Homeostasis and Disease. Biomolecules 2020, 10, 1211. [Google Scholar] [CrossRef]
- Tain, Y.L.; Leu, S.; Wu, K.L.; Lee, W.C.; Chan, J.Y. Melatonin prevents maternal fructose intake-induced programmed hypertension in the offspring: Roles of nitric oxide and arachidonic acid metabolites. J. Pineal Res. 2014, 57, 80–89. [Google Scholar]
- Andersen, L.P.; Gögenur, I.; Rosenberg, J.; Reiter, R.J. The Safety of Melatonin in Humans. Clin. Drug Investig. 2016, 36, 169–175. [Google Scholar]
- Korkmaz, A.; Rosales-Corral, S.; Reiter, R.J. Gene regulation by melatonin linked to epigenetic phenomena. Gene 2012, 503, 1–11. [Google Scholar]
- Linowiecka, K.; Slominski, A.T.; Reiter, R.J.; Böhm, M.; Steinbrink, K.; Paus, R.; Kleszczyński, K. Melatonin: A Potential Regulator of DNA Methylation. Antioxidants 2023, 12, 1155. [Google Scholar] [CrossRef] [PubMed]
- Salamon, S.; Kramar, B.; Marolt, T.P.; Poljšak, B.; Milisav, I. Medical and Dietary Uses of N-Acetylcysteine. Antioxidants 2019, 8, 111. [Google Scholar] [CrossRef] [PubMed]
- Kimura, H. The physiological role of hydrogen sulfide and beyond. Nitric Oxide 2014, 41, 4–10. [Google Scholar] [PubMed]
- Plotnikov, E.Y.; Pavlenko, T.A.; Pevzner, I.B.; Zorova, L.D.; Manskikh, V.N.; Silachev, D.N. The role of oxidative stress in acute renal injury of newborn rats exposed to hypoxia and endotoxin. FEBS J. 2017, 284, 3069–3078. [Google Scholar]
- Johnson, S.T.; Bigam, D.L.; Emara, M.; Obaid, L.; Slack, G.; Korbutt, G. N-acetylcysteine improves the hemodynamics and oxidative stress in hypoxic newborn pigs reoxygenated with 100% oxygen. Shock 2007, 28, 484–490. [Google Scholar]
- Tai, I.H.; Sheen, J.M.; Lin, Y.J.; Yu, H.R.; Tiao, M.M.; Chen, C.C.; Huang, L.T.; Tain, Y.L. Maternal N-acetylcysteine therapy regulates hydrogen sulfide-generating pathway and prevents programmed hypertension in male offspring exposed to prenatal dexamethasone and postnatal high-fat diet. Nitric Oxide 2016, 53, 6–12. [Google Scholar]
- James, A.M.; Smith, R.A.; Murphy, M.P. Antioxidant and prooxidant properties of mitochondrial Coenzyme Q. Arch. Biochem. Biophys. 2004, 423, 47–56. [Google Scholar]
- Tintoré, M.; Sastre-Garriga, J. Multiple sclerosis: Dimethyl fumarate is coming of age. Nat. Rev. Neurol. 2016, 12, 436–437. [Google Scholar]
- Hsu, C.N.; Lin, Y.J.; Yu, H.R.; Lin, I.C.; Sheen, J.M.; Huang, L.T.; Tain, Y.L. Protection of Male Rat Offspring against Hypertension Programmed by Prenatal Dexamethasone Administration and Postnatal High-Fat Diet with the Nrf2 Activator Dimethyl Fumarate during Pregnancy. Int. J. Mol. Sci. 2019, 20, 3957. [Google Scholar] [CrossRef]
- Rosa, A.C.; Corsi, D.; Cavi, N.; Bruni, N.; Dosio, F. Superoxide Dismutase Administration: A Review of Proposed Human Uses. Molecules 2021, 26, 1844. [Google Scholar] [CrossRef]
- Koeners, M.P.; Braam, B.; Joles, J.A. Perinatal inhibition of NF-kappaB has long-term antihypertensive effects in spontaneously hypertensive rats. J. Hypertens. 2011, 29, 1160–1166. [Google Scholar] [CrossRef] [PubMed]
- Goss, S.P.; Kalyanaraman, B.; Hogg, N. Antioxidant effects of nitric oxide and nitric oxide donor compounds on low-density lipoprotein oxidation. Methods Enzymol. 1999, 301, 444–453. [Google Scholar] [PubMed]
- Andrabi, S.M.; Sharma, N.S.; Karan, A.; Shahriar, S.M.S.; Cordon, B.; Ma, B.; Xie, J. Nitric Oxide: Physiological Functions, Delivery, and Biomedical Applications. Adv. Sci. 2023, 10, e2303259. [Google Scholar] [CrossRef] [PubMed]
- Teerlink, T.; Luo, Z.; Palm, F.; Wilcox, C.S. Cellular ADMA: Regulation and action. Pharmacol. Res. 2009, 60, 448–460. [Google Scholar] [CrossRef]
- Beltowski, J.; Kedra, A. Asymmetric dimethylarginine (ADMA) as a target for pharmacotherapy. Pharmacol. Rep. 2006, 58, 159–178. [Google Scholar]
- Onozato, M.L.; Tojo, A.; Leiper, J.; Fujita, T.; Palm, F.; Wilcox, C.S. Expression of NG,NG-dimethylarginine dimethylaminohydrolase and protein arginine N-methyltransferase isoforms in diabetic rat kidney: Effects of angiotensin II receptor blockers. Diabetes 2008, 57, 172–180. [Google Scholar] [CrossRef]
- Ojima, A.; Ishibashi, Y.; Matsui, T.; Maeda, S.; Nishino, Y.; Takeuchi, M.; Fukami, K.; Yamagishi, S. Glucagon-like peptide-1 receptor agonist inhibits asymmetric dimethylarginine generation in the kidney of streptozotocin-induced diabetic rats by blocking advanced glycation end product-induced protein arginine methyltranferase-1 expression. Am. J. Pathol. 2013, 182, 132–141. [Google Scholar] [CrossRef]
- Sicard, P.; Delemasure, S.; Korandji, C.; Segueira-Le Grand, A.; Lauzier, B.; Guilland, J.C.; Duvillard, L.; Zeller, M.; Cottin, Y.; Vergely, C.; et al. Anti-hypertensive effects of Rosuvastatin are associated with decreased inflammation and oxidative stress markers in hypertensive rats. Free Radic. Res. 2008, 42, 226–236. [Google Scholar] [CrossRef]
- Chen, D.; Zhang, K.Q.; Li, B.; Sun, D.Q.; Zhang, H.; Fu, Q. Epigallocatechin-3-gallate ameliorates erectile function in aged rats via regulation of PRMT1/DDAH/ADMA/NOS metabolism pathway. Asian J. Androl. 2017, 19, 291–297. [Google Scholar]
- Bal, F.; Bekpinar, S.; Unlucerci, Y.; Kusku-Kiraz, Z.; Önder, S.; Uysal, M.; Gurdol, F. Antidiabetic drug metformin is effective on the metabolism of asymmetric dimethylarginine in experimental liver injury. Diabetes Res. Clin. Pract. 2014, 106, 295–302. [Google Scholar] [CrossRef]
- Zheng, D.; Liang, Q.; Zeng, F.; Mai, Z.; Cai, A.; Qiu, R.; Xu, R.; Li, D.; Mai, W. Atorvastatin protects endothelium by decreasing asymmetric dimethylarginine in dyslipidemia rats. Lipids Health Dis. 2015, 14, 41. [Google Scholar] [CrossRef] [PubMed]
- He, H.; Li, X.; Wang, H.; Zhang, W.; Jiang, H.; Wang, S.; Yuan, L.; Liu, Y.; Liu, X. Effects of salvianolic acid A on plasma and tissue dimethylarginine levels in a rat model of myocardial infarction. J. Cardiovasc. Pharmacol. 2013, 61, 482–488. [Google Scholar] [PubMed]
- Zhang, W.; Zhang, J.; Liu, Y.K.; Liu, J.; Wang, X.; Xu, Q.; Wang, Y.; Xu, X.; Dai, G. Cardioprotective effects of oxymatrine on isoproterenol-induced heart failure via regulation of DDAH/ADMA metabolism pathway in rats. Eur. J. Pharmacol. 2014, 745, 29–35. [Google Scholar] [CrossRef] [PubMed]
- Hu, T.; Chouinard, M.; Cox, A.L.; Sipes, P.; Marcelo, M.; Ficorilli, J.; Li, S.; Gao, H.; Ryan, T.P.; Michael, M.D.; et al. Farnesoid X receptor agonist reduces serum asymmetric dimethylarginine levels through hepatic dimethylarginine dimethylaminohydrolase-1 gene regulation. J. Biol. Chem. 2006, 281, 39831–39838. [Google Scholar]
- Wang, Y.; Zhang, M.; Liu, Y.; Liu, Y.; Chen, M. The effect of nebivolol on asymmetric dimethylarginine system in spontaneously hypertension rats. Vascul. Pharmacol. 2011, 54, 36–43. [Google Scholar]
- Wang, K.; Wang, Y.; Zhang, H.; Li, X.; Han, W. A Review of the Synthesis of Nitric Oxide Donor and Donor Derivatives with Pharmacological Activities. Mini. Rev. Med. Chem. 2022, 22, 873–883. [Google Scholar]
- Bonini, M.G.; Stadler, K.; Silva, S.O.; Corbett, J.; Dore, M.; Petranka, J.; Fernandes, D.C.; Tanaka, L.Y.; Duma, D.; Laurindo, F.R.; et al. Constitutive nitric oxide synthase activation is a significant route for nitroglycerin-mediated vasodilation. Proc. Natl. Acad. Sci. USA 2008, 105, 8569–8574. [Google Scholar]
- Liu, T.; Schroeder, H.; Power, G.G.; Blood, A.B. A physiologically relevant role for NO stored in vascular smooth muscle cells: A novel theory of vascular NO signaling. Redox Biol. 2022, 53, 102327. [Google Scholar]
- Wu, Z.; Siuda, D.; Xia, N.; Reifenberg, G.; Daiber, A.; Münzel, T.; Förstermann, U.; Li, H. Maternal treatment of spontaneously hypertensive rats with pentaerythritoltetranitrate reduces blood pressure in female offspring. Hypertension 2015, 65, 232–237. [Google Scholar] [CrossRef]
- Wesseling, S.; Essers, P.B.; Koeners, M.P.; Pereboom, T.C.; Braam, B.; van Faassen, E.E.; Macinnes, A.W.; Joles, J.A. Perinatal exogenous nitric oxide in fawn-hooded hypertensive rats reduces renal ribosomal biogenesis in early life. Front. Genet. 2011, 2, 52. [Google Scholar] [CrossRef]
- Magliocca, G.; Mone, P.; Di Iorio, B.R.; Heidland, A.; Marzocco, S. Short-Chain Fatty Acids in Chronic Kidney Disease: Focus on Inflammation and Oxidative Stress Regulation. Int. J. Mol. Sci. 2022, 23, 5354. [Google Scholar] [CrossRef] [PubMed]
- Rekha, K.; Venkidasamy, B.; Samynathan, R.; Nagella, P.; Rebezov, M.; Khayrullin, M.; Ponomarev, E.; Bouyahya, A.; Sarkar, T.; Shariati, M.A.; et al. Short-chain fatty acid: An updated review on signaling, metabolism, and therapeutic effects. Crit. Rev. Food Sci. Nutr. 2024, 64, 2461–2489. [Google Scholar] [CrossRef] [PubMed]
- Valvassori, S.S.; Dal-Pont, G.C.; Steckert, A.V.; Varela, R.B.; Lopes-Borges, J.; Mariot, E.; Resende, W.R.; Arent, C.O.; Carvalho, A.F.; Quevedo, J. Sodium butyrate has an antimanic effect and protects the brain against oxidative stress in an animal model of mania induced by ouabain. Psychiatry Res. 2016, 235, 154–159. [Google Scholar] [CrossRef] [PubMed]
- Ziętek, M.; Celewicz, Z.; Szczuko, M. Short-Chain Fatty Acids, Maternal Microbiota and Metabolism in Pregnancy. Nutrients 2021, 13, 1244. [Google Scholar] [CrossRef]
- Hsu, C.N.; Tain, Y.L. Chronic Kidney Disease and Gut Microbiota: What Is Their Connection in Early Life? Int. J. Mol. Sci. 2022, 23, 3954. [Google Scholar] [CrossRef]
- Hsu, C.N.; Tain, Y.L. Targeting the Renin-Angiotensin-Aldosterone System to Prevent Hypertension and Kidney Disease of Developmental Origins. Int. J. Mol. Sci. 2021, 22, 2298. [Google Scholar] [CrossRef]
- Chavatte-Palmer, P.; Tarrade, A.; Rousseau-Ralliard, D. Diet before and during Pregnancy and Offspring Health: The Importance of Animal Models and What Can Be Learned from Them. Int. J. Environ. Res. Public Health 2016, 13, 586. [Google Scholar] [CrossRef]
- Furukawa, S.; Kuroda, Y.; Sugiyama, A. A comparison of the histological structure of the placenta in experimental animals. J. Toxicol. Pathol. 2014, 27, 11–18. [Google Scholar] [CrossRef]
- Morel, O.; Laporte-Broux, B.; Tarrade, A.; Chavatte-Palmer, P. The use of ruminant models in biomedical perinatal research. Theriogenology 2012, 78, 1763–1773. [Google Scholar] [CrossRef]
- Zhang, Y.; Li, Y.; Ren, T.; Duan, J.A.; Xiao, P. Promising tools into oxidative stress: A review of non-rodent model organisms. Redox Biol. 2024, 77, 103402. [Google Scholar] [CrossRef]
- Demirci-Çekiç, S.; Özkan, G.; Avan, A.N.; Uzunboy, S.; Çapanoğlu, E.; Apak, R. Biomarkers of Oxidative Stress and Antioxidant Defense. J Pharm Biomed Anal. 2022, 209, 114477. [Google Scholar]
- Suzen, S.; Gurer-Orhan, H.; Saso, L. Detection of Reactive Oxygen and Nitrogen Species by Electron Paramagnetic Resonance (EPR) Technique. Molecules 2017, 22, 181. [Google Scholar] [CrossRef] [PubMed]
- ClinicalTrials.gov. 2022. Available online: https://clinicaltrials.gov/ (accessed on 10 March 2025).
- Yuksel, S.; Yigit, A.A.; Cinar, M.; Atmaca, N.; Onaran, Y. Oxidant and Antioxidant Status of Human Breast Milk during Lactation Period. Dairy. Sci. Technol. 2015, 95, 295–302. [Google Scholar] [CrossRef]
- Khan, I.T.; Nadeem, M.; Imran, M.; Ullah, R.; Ajmal, M.; Jaspal, M.H. Antioxidant properties of Milk and dairy products: A comprehensive review of the current knowledge. Lipids Health Dis. 2019, 18, 41. [Google Scholar]
- Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics 2012, 129, e827–e841. [Google Scholar] [CrossRef]
- Sotler, R.; Poljšak, B.; Dahmane, R.; Jukić, T.; Pavan Jukić, D.; Rotim, C.; Trebše, P.; Starc, A. Prooxidant activities of antioxidants and their impact on health. Acta Clin. Croat. 2019, 58, 726–736. [Google Scholar]
- Carlisle, D.L.; Pritchard, D.E.; Singh, J.; Owens, B.M.; Blankenship, L.J.; Orenstein, J.M.; Patierno, S.R. Apoptosis and P53 induction in human lung fibroblasts exposed to chromium (VI): Effect of ascorbate and tocopherol. Toxicol. Sci. 2000, 55, 60–68. [Google Scholar]
- Halliwell, B. The antioxidant paradox. Lancet 2000, 355, 1179–1180. [Google Scholar]
- Henderson, J.T.; Thompson, J.H.; Burda, B.U.; Cantor, A. Preeclampsia Screening: Evidence Report and Systematic Review for the US Preventive Services Task Force. JAMA 2017, 317, 1668–1683. [Google Scholar]
- Ahmed, R.; Dunford, J.; Mehran, R.; Robson, S.; Kunadian, V. Pre-eclampsia and future cardiovascular risk among women: A review. J. Am. Coll. Cardiol. 2014, 63, 1815–1822. [Google Scholar]
- Mosimann, B.; Amylidi-Mohr, S.K.; Surbek, D.; Raio, L. First trimester screening for preeclampsia—A systematic review. Hypertens. Pregnancy 2020, 39, 1–11. [Google Scholar] [PubMed]
Animal Models | Species | Programming Exposure | Mechanisms of Oxidative Stress | Ref. |
---|---|---|---|---|
Nutrient manipulation | Rat | Caloric restriction | ↓ NO, ↑ Kidney oxidative damage | [65,66] |
Rat | Protein restriction | ↑ Oxidative damage, ↓ Antioxidant capabilities | [67] | |
Rat | High-fructose diet | ↓ NO, ↑ Kidney oxidative damage | [68] | |
Rat | Methyl-deficient diet | ↑ Kidney oxidative damage | [69] | |
Rat | High-methyl-donor diet | ↑ Kidney oxidative damage | [69] | |
Rat | Low-iron diet | ↑ Kidney oxidative damage | [70] | |
Rat | High-fat diet | ↓ NO, ↑ Kidney oxidative damage, ↓ Antioxidant capabilities | [71,72,73] | |
Mouse | High-fat diet | ↑ Kidney oxidative damage, ↑ ROS-generating enzymes | [74,75] | |
Surgical intervention | Rat | Reduced uterine perfusion | ↑ Kidney oxidative damage, ↑ ROS | [76] |
Pharmacological intervention | Rat | Diabetes induced by streptozotocin | ↓ NO, ↑ Kidney oxidative damage | [77,78] |
Rat | Preeclampsia induced by L-NAME | ↑ Kidney oxidative damage | [79] | |
Rat | Preeclampsia induced by suramin | ↓ NO | [80] | |
Rat | CKD induced by adenine | ↓ NO, ↑ Kidney oxidative damage | [81,82] | |
Rat | Endothelial dysfunction induced by angiotensin II | ↑ ROS | [83] | |
Rat | Endothelial dysfunction induced by ADMA | ↓ NO | [84] | |
Rat | LPS administration | ↑ Kidney oxidative damage | [85,86] | |
Rat | Antenatal glucocorticoids | ↓ NO, ↑ Kidney oxidative damage, ↓ Antioxidant capabilities | [87,88] | |
Sheep | Antenatal glucocorticoids | ↓ NO, ↑ ROS | [89] | |
Pollution exposure | Mouse | Maternal nicotine exposure | ↑ Kidney ROS | [90] |
Rat | Maternal di-n-butyl phthalate exposure | ↑ Kidney ROS | [91] | |
Rat | Maternal bisphenol A exposure plus high-fat diet | ↓ NO, ↑Kidney oxidative damage | [92] | |
Rat | Prenatal TCDD plus dexamethasone exposure | ↑Kidney oxidative damage, ↓ NO | [93] |
Key Research Gap | Summary |
---|---|
Challenges in manipulating redox status during gestation |
|
| |
Organ-specific vulnerability |
|
| |
Limitations of rodent models |
|
| |
Methodological challenges in assessing oxidative stress |
|
| |
Antioxidant interventions |
|
| |
Safety concerns with antioxidants |
|
| |
Long-term impact on kidney health |
|
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lu, P.-C.; Tain, Y.-L.; Lin, Y.-J.; Hsu, C.-N. Oxidative Stress in Maternal and Offspring Kidney Disease and Hypertension: A Life-Course Perspective. Antioxidants 2025, 14, 387. https://doi.org/10.3390/antiox14040387
Lu P-C, Tain Y-L, Lin Y-J, Hsu C-N. Oxidative Stress in Maternal and Offspring Kidney Disease and Hypertension: A Life-Course Perspective. Antioxidants. 2025; 14(4):387. https://doi.org/10.3390/antiox14040387
Chicago/Turabian StyleLu, Pei-Chen, You-Lin Tain, Ying-Jui Lin, and Chien-Ning Hsu. 2025. "Oxidative Stress in Maternal and Offspring Kidney Disease and Hypertension: A Life-Course Perspective" Antioxidants 14, no. 4: 387. https://doi.org/10.3390/antiox14040387
APA StyleLu, P.-C., Tain, Y.-L., Lin, Y.-J., & Hsu, C.-N. (2025). Oxidative Stress in Maternal and Offspring Kidney Disease and Hypertension: A Life-Course Perspective. Antioxidants, 14(4), 387. https://doi.org/10.3390/antiox14040387