The Mechanism of Hyperoxia-Induced Neonatal Renal Injury and the Possible Protective Effect of Resveratrol

Abstract

With recent advances in neonatal intensive care, preterm infants are surviving into adulthood. Nonetheless, epidemiological data on the health status of these preterm infants have begun to reveal a worrying theme; prematurity and the supplemental oxygen therapy these infants receive after birth appear to be risk factors for kidney disease in adulthood, affecting their quality of life. As the incidence of chronic kidney disease and the survival time of preterm infants both increase, the management of the hyperoxia-induced renal disease is becoming increasingly relevant to neonatologists. The mechanism of this increased risk is currently unknown, but prematurity itself and hyperoxia exposure after birth may predispose to disease by altering the normal trajectory of kidney maturation. This article reviews altered renal reactivity due to hyperoxia, the possible mechanisms of renal injury due to hyperoxia, and the role of resveratrol in renal injury.

Key Points

• Premature infants commonly receive supplementary oxygen.

• Hyperoxia can cause kidney damage via signal pathways.

• We should reduce the occurrence of late sequelae.

Keywords

resveratrol - hyperoxia - renal injury - CKD

Authors' Contributions

Y.S. wrote the manuscript. Y.Y. provides support in investigation and data collation. W.D. audited the manuscript. All authors contributed to the article and approved the submitted version.

Publication History

Received: 29 August 2021

Accepted: 17 March 2022

Accepted Manuscript online:
05 April 2022

Article published online:
04 July 2022

• References

• 1 Zhu Y, Fu J, Yang H, Pan Y, Yao L, Xue X. Hyperoxia-induced methylation decreases RUNX3 in a newborn rat model of bronchopulmonary dysplasia. Respir Res 2015; 16 (01) 75
• 2 Richter AE, Bos AF, Huiskamp EA, Kooi EMW. Postnatal cerebral hyperoxia is associated with an increased risk of severe retinopathy of prematurity. Neonatology 2019; 116 (04) 356-362
• 3 Yiş U, Kurul SH, Kumral A. et al. Hyperoxic exposure leads to cell death in the developing brain. Brain Dev 2008; 30 (09) 556-562
• 4 Ramani M, van Groen T, Kadish I, Bulger A, Ambalavanan N. Neurodevelopmental impairment following neonatal hyperoxia in the mouse. Neurobiol Dis 2013; 50: 69-75
• 5 Ritter J, Schmitz T, Chew LJ. et al. Neonatal hyperoxia exposure disrupts axon-oligodendrocyte integrity in the subcortical white matter. J Neurosci 2013; 33 (21) 8990-9002
• 6 Schmitz T, Ritter J, Mueller S, Felderhoff-Mueser U, Chew LJ, Gallo V. Cellular changes underlying hyperoxia-induced delay of white matter development. J Neurosci 2011; 31 (11) 4327-4344
• 7 Klinger G, Beyene J, Shah P, Perlman M. Do hyperoxaemia and hypocapnia add to the risk of brain injury after intrapartum asphyxia?. Arch Dis Child Fetal Neonatal Ed 2005; 90 (01) F49-F52
• 8 Shimabuku R, Ota A, Pereyra S. et al. Hyperoxia with 100% oxygen following hypoxia-ischemia increases brain damage in newborn rats. Biol Neonate 2005; 88 (03) 168-171
• 9 Collins MP, Lorenz JM, Jetton JR, Paneth N. Hypocapnia and other ventilation-related risk factors for cerebral palsy in low birth weight infants. Pediatr Res 2001; 50 (06) 712-719
• 10 Rawat D, Shrivastava S, Naik RA, Chhonker SK, Koiri RK. SIRT1-mediated amelioration of oxidative stress in kidney of alcohol-aflatoxin-B1-induced hepatocellular carcinoma by resveratrol is catalase dependent and GPx independent. J Biochem Mol Toxicol 2020; 34 (11) e22576
• 11 Pei J, Cai S, Song S. et al. Normobaric hyperoxia plays a protective role against renal ischemia-reperfusion injury by activating the Nrf2/HO-1 signaling pathway. Biochem Biophys Res Commun 2020; 532 (01) 151-158
• 12 Calzia E, Asfar P, Hauser B. et al. Hyperoxia may be beneficial. Crit Care Med 2010; 38 (10, Suppl): S559-S568
• 13 Knöller E, Stenzel T, Broeskamp F. et al. Effects of hyperoxia and mild therapeutic hypothermia during resuscitation from porcine hemorrhagic shock. Crit Care Med 2016; 44 (05) e264-e277
• 14 Jiang JS, Chou HC, Yeh TF, Chen CM. Neonatal hyperoxia exposure induces kidney fibrosis in rats. Pediatr Neonatol 2015; 56 (04) 235-241
• 15 Chen CM, Hwang J, Chou HC. Immunization with anti-Tn immunogen in maternal rats protects against hyperoxia-induced kidney injury in newborn offspring. Pediatr Res 2021; 89 (03) 476-482
• 16 Chou HC, Chen CM. Cathelicidin attenuates hyperoxia-induced kidney injury in newborn rats. Ren Fail 2019; 41 (01) 733-741
• 17 Sutherland MR, Béland C, Lukaszewski MA, Cloutier A, Bertagnolli M, Nuyt AM. Age- and sex-related changes in rat renal function and pathology following neonatal hyperoxia exposure. Physiol Rep 2016; 4 (15) e12887
• 18 Sutherland MR, O'Reilly M, Kenna K. et al. Neonatal hyperoxia: effects on nephrogenesis and long-term glomerular structure. Am J Physiol Renal Physiol 2013; 304 (10) F1308-F1316
• 19 Stritzke A, Thomas S, Amin H, Fusch C, Lodha A. Renal consequences of preterm birth. Mol Cell Pediatr 2017; 4 (01) 2
• 20 Starr MC, Hingorani SR. Prematurity and future kidney health: the growing risk of chronic kidney disease. Curr Opin Pediatr 2018; 30 (02) 228-235
• 21 Popescu CR, Sutherland MR, Cloutier A. et al. Hyperoxia exposure impairs nephrogenesis in the neonatal rat: role of HIF-1α. PLoS One 2013; 8 (12) e82421
• 22 Goldstein RS, Tarloff JB, Hook JB. Age-related nephropathy in laboratory rats. FASEB J 1988; 2 (07) 2241-2251
• 23 Reckelhoff JF. Age-related changes in renal hemodynamics in female rats: role of multiple pregnancy and NO. Am J Physiol 1997; 272 (6 Pt 2): R1985-R1989
• 24 Vento M, Sastre J, Asensi MA, Viña J. Room-air resuscitation causes less damage to heart and kidney than 100% oxygen. Am J Respir Crit Care Med 2005; 172 (11) 1393-1398
• 25 Perrone S, Mussap M, Longini M. et al. Oxidative kidney damage in preterm newborns during perinatal period. Clin Biochem 2007; 40 (9-10): 656-660
• 26 Black MJ, Lim K, Zimanyi MA. et al. Accelerated age-related decline in renal and vascular function in female rats following early-life growth restriction. Am J Physiol Regul Integr Comp Physiol 2015; 309 (09) R1153-R1161
• 27 Keijzer-Veen MG, Schrevel M, Finken MJ. et al; Dutch POPS-19 Collaborative Study Group. Microalbuminuria and lower glomerular filtration rate at young adult age in subjects born very premature and after intrauterine growth retardation. J Am Soc Nephrol 2005; 16 (09) 2762-2768
• 28 Bacchetta J, Harambat J, Dubourg L. et al. Both extrauterine and intrauterine growth restriction impair renal function in children born very preterm. Kidney Int 2009; 76 (04) 445-452
• 29 Sen N, Satija YK, Das S. PGC-1α, a key modulator of p53, promotes cell survival upon metabolic stress. Mol Cell 2011; 44 (04) 621-634
• 30 Dalziel SR, Parag V, Rodgers A, Harding JE. Cardiovascular risk factors at age 30 following pre-term birth. Int J Epidemiol 2007; 36 (04) 907-915
• 31 Cooper R, Atherton K, Power C. Gestational age and risk factors for cardiovascular disease: evidence from the 1958 British birth cohort followed to mid-life. Int J Epidemiol 2009; 38 (01) 235-244
• 32 de Jong F, Monuteaux MC, van Elburg RM, Gillman MW, Belfort MB. Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension 2012; 59 (02) 226-234
• 33 Gerdin E, Tydén O, Eriksson UJ. The development of antioxidant enzymatic defense in the perinatal rat lung: activities of superoxide dismutase, glutathione peroxidase, and catalase. Pediatr Res 1985; 19 (07) 687-691
• 34 Dyson A, Kent AL. The effect of preterm birth on renal development and renal health outcome. Neoreviews 2019; 20 (12) e725-e736
• 35 Yen CC, Chang WH, Tung MC. et al. Lactoferrin protects hyperoxia-induced lung and kidney systemic inflammation in an in vivo imaging model of NF-κB/luciferase transgenic mice. Mol Imaging Biol 2020; 22 (03) 526-538
• 36 Noronha IL, Fujihara CK, Zatz R. The inflammatory component in progressive renal disease–are interventions possible?. Nephrol Dial Transplant 2002; 17 (03) 363-368
• 37 Saldanha JF, Leal VdeO, Stenvinkel P, Carraro-Eduardo JC, Mafra D. Resveratrol: why is it a promising therapy for chronic kidney disease patients?. Oxid Med Cell Longev 2013; 2013: 963217
• 38 Sucre JMS, Vickers KC, Benjamin JT. et al. Hyperoxia injury in the developing lung is mediated by mesenchymal expression of Wnt5A. Am J Respir Crit Care Med 2020; 201 (10) 1249-1262
• 39 Ali MF, Venkatarayappa SKB, Benny M. et al. Effects of klotho supplementation on hyperoxia-induced renal injury in a rodent model of postnatal nephrogenesis. Pediatr Res 2020; 88 (04) 565-570
• 40 Mohr J, Voggel J, Vohlen C. et al. IL-6/Smad2 signaling mediates acute kidney injury and regeneration in a murine model of neonatal hyperoxia. FASEB J 2019; 33 (05) 5887-5902
• 41 Beshay ON, Ewees MG, Abdel-Bakky MS, Hafez SMNA, Abdelrehim AB, Bayoumi AMA. Resveratrol reduces gentamicin-induced EMT in the kidney via inhibition of reactive oxygen species and involving TGF-β/Smad pathway. Life Sci 2020; 258: 118178
• 42 Smeeton J, Zhang X, Bulus N. et al. Integrin-linked kinase regulates p38 MAPK-dependent cell cycle arrest in ureteric bud development. Development 2010; 137 (19) 3233-3243
• 43 Ihermann-Hella A, Hirashima T, Kupari J. et al. Dynamic MAPK/ERK activity sustains nephron progenitors through niche regulation and primes precursors for differentiation. Stem Cell Reports 2018; 11 (04) 912-928
• 44 Xu X, You K, Bu R. Proximal tubular development is impaired with downregulation of MAPK/ERK signaling, HIF-1α, and catalase by hyperoxia exposure in neonatal rats. Oxid Med Cell Longev 2019; 2019: 9219847
• 45 Xu X, Zhang X, Gao L, Liu C, You K. Neonatal hyperoxia downregulates claudin-4, occludin, and ZO-1 expression in rat kidney accompanied by impaired proximal tubular development. Oxid Med Cell Longev 2020; 2020: 2641461
• 46 Yzydorczyk C, Comte B, Cambonie G. et al. Neonatal oxygen exposure in rats leads to cardiovascular and renal alterations in adulthood. Hypertension 2008; 52 (05) 889-895
• 47 Liu D, Wang Y, Li L. et al. Celecoxib protects hyperoxia-induced lung injury via NF-κB and AQP1. Front Pediatr 2019; 7: 228
• 48 Seyahian EA, Cacciagiu L, Damiano AE, Zotta E. AQP1 expression in the proximal tubule of diabetic rat kidney. Heliyon 2020; 6 (01) e03192
• 49 de Almeida LF, Coimbra TM. Neonatal hyperoxia: effects on nephrogenesis and the key role of klotho as an antioxidant factor. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet 2022; 35 (15) 3020-2
• 50 Gilfillan M, Das P, Shah D, Alam MA, Bhandari V. Inhibition of microRNA-451 is associated with increased expression of Macrophage Migration Inhibitory Factor and mitgation of the cardio-pulmonary phenotype in a murine model of bronchopulmonary dysplasia. Respir Res 2020; 21 (01) 92
• 51 Sun H, Choo-Wing R, Fan J. et al. Small molecular modulation of macrophage migration inhibitory factor in the hyperoxia-induced mouse model of bronchopulmonary dysplasia. Respir Res 2013; 14 (01) 27
• 52 Mammoto T, Chen J, Jiang E. et al. LRP5 regulates development of lung microvessels and alveoli through the angiopoietin-Tie2 pathway. PLoS One 2012; 7 (07) e41596
• 53 Ruan Y, Dong W, Kang L. et al. The changes of Twist1 pathway in pulmonary microvascular permeability in a newborn rat model of hyperoxia-induced acute lung injury. Front Pediatr 2020; 8: 190
• 54 Nakagawa M, Nishizaki N, Endo A. et al. Impaired nephrogenesis in neonatal rats with oxygen-induced retinopathy. Pediatr Int (Roma) 2017; 59 (06) 704-710
• 55 GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016; 388 (10053): 1459-1544
• 56 Saran R, Robinson B, Abbott KC. et al. US renal data system 2019 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis 2020; 75 (01, Suppl 1): A6-A7
• 57 Liu KD, Brakeman PR. Renal repair and recovery. Crit Care Med 2008; 36 (04) S187-S192
• 58 Zhao L, Hu C, Zhang P, Jiang H, Chen J. Melatonin preconditioning is an effective strategy for mesenchymal stem cell-based therapy for kidney disease. J Cell Mol Med 2020; 24 (01) 25-33
• 59 Little MH, Kairath P. Regenerative medicine in kidney disease. Kidney Int 2016; 90 (02) 289-299
• 60 Klomjit N, Lerman A, Lerman LO. It comes as a shock: kidney repair using shockwave therapy. Hypertension 2020; 76 (06) 1696-1703
• 61 Groopman EE, Rasouly HM, Gharavi AG. Genomic medicine for kidney disease. Nat Rev Nephrol 2018; 14 (02) 83-104
• 62 Cruz NM, Freedman BS. CRISPR gene editing in the kidney. Am J Kidney Dis 2018; 71 (06) 874-883
• 63 Doyle R, Godson C, Brennan E. Promoting resolution in kidney disease: are we nearly there yet?. Curr Opin Nephrol Hypertens 2020; 29 (01) 119-127
• 64 Geng X, Zhong D, Su L, Lin Z, Yang B. Preventive and therapeutic effect of Ganoderma lucidum on kidney injuries and diseases. Adv Pharmacol 2020; 87: 257-276
• 65 Den Hartogh DJ, Tsiani E. Health benefits of resveratrol in kidney disease: evidence from in vitro and in vivo studies. Nutrients 2019; 11 (07) E1624
• 66 Yuan D, Liu XM, Fang Z, Du LL, Chang J, Lin SH. Protective effect of resveratrol on kidney in rats with diabetic nephropathy and its effect on endoplasmic reticulum stress. Eur Rev Med Pharmacol Sci 2018; 22 (05) 1485-1493
• 67 Park HS, Lim JH, Kim MY. et al. Resveratrol increases AdipoR1 and AdipoR2 expression in type 2 diabetic nephropathy. J Transl Med 2016; 14 (01) 176
• 68 Jo SK, Ko GJ, Boo CS, Cho WY, Kim HK. Heat preconditioning attenuates renal injury in ischemic ARF in rats: role of heat-shock protein 70 on NF-kappaB-mediated inflammation and on tubular cell injury. J Am Soc Nephrol 2006; 17 (11) 3082-3092
• 69 Feng S, Wang J, Teng J, Fang Z, Lin C. Resveratrol plays protective roles on kidney of uremic rats via activating HSP70 expression. BioMed Res Int 2020; 2020: 2126748
• 70 Rauf A, Imran M, Butt MS, Nadeem M, Peters DG, Mubarak MS. Resveratrol as an anti-cancer agent: a review. Crit Rev Food Sci Nutr 2018; 58 (09) 1428-1447
• 71 Wang Y, Feng F, Liu M, Xue J, Huang H. Resveratrol ameliorates sepsis-induced acute kidney injury in a pediatric rat model via Nrf2 signaling pathway. Exp Ther Med 2018; 16 (04) 3233-3240
• 72 Kim EN, Lim JH, Kim MY. et al. Resveratrol, an Nrf2 activator, ameliorates aging-related progressive renal injury. Aging (Albany NY) 2018; 10 (01) 83-99
• 73 Li P, Song X, Zhang D. et al. Resveratrol improves left ventricular remodeling in chronic kidney disease via Sirt1-mediated regulation of FoxO1 activity and MnSOD expression. Biofactors 2020; 46 (01) 168-179
• 74 Kim EN, Lim JH, Kim MY. et al. PPARα agonist, fenofibrate, ameliorates age-related renal injury. Exp Gerontol 2016; 81: 42-50
• 75 Hui Y, Lu M, Han Y. et al. Resveratrol improves mitochondrial function in the remnant kidney from 5/6 nephrectomized rats. Acta Histochem 2017; 119 (04) 392-399
• 76 Zhang Q, Zhang C, Ge J. et al. Ameliorative effects of resveratrol against cadmium-induced nephrotoxicity via modulating nuclear xenobiotic receptor response and PINK1/Parkin-mediated Mitophagy. Food Funct 2020; 11 (02) 1856-1868
• 77 Wang Y, Wang B, Qi X, Zhang X, Ren K. Resveratrol protects against post-contrast acute kidney injury in rabbits with diabetic nephropathy. Front Pharmacol 2019; 10: 833
• 78 Hasegawa K, Wakino S, Yoshioka K. et al. Kidney-specific overexpression of Sirt1 protects against acute kidney injury by retaining peroxisome function. J Biol Chem 2010; 285 (17) 13045-13056
• 79 He W, Wang Y, Zhang MZ. et al. Sirt1 activation protects the mouse renal medulla from oxidative injury. J Clin Invest 2010; 120 (04) 1056-1068
• 80 Kume S, Uzu T, Horiike K. et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest 2010; 120 (04) 1043-1055
• 81 Kim MY, Lim JH, Youn HH. et al. Resveratrol prevents renal lipotoxicity and inhibits mesangial cell glucotoxicity in a manner dependent on the AMPK-SIRT1-PGC1α axis in db/db mice. Diabetologia 2013; 56 (01) 204-217
• 82 Zhong Y, Lee K, He JC. SIRT1 is a potential drug target for treatment of diabetic kidney disease. Front Endocrinol (Lausanne) 2018; 9: 624
• 83 Bao N, Chen F, Dai D. The regulation of host intestinal microbiota by polyphenols in the development and prevention of chronic kidney disease. Front Immunol 2020; 10: 2981
• 84 Yang K, Dong W. Perspectives on probiotics and bronchopulmonary dysplasia. Front Pediatr 2020; 8: 570247
• 85 Carrera-Quintanar L, López Roa RI, Quintero-Fabián S, Sánchez-Sánchez MA, Vizmanos B, Ortuño-Sahagún D. Phytochemicals that influence gut microbiota as prophylactics and for the treatment of obesity and inflammatory diseases. Mediators Inflamm 2018; 2018: 9734845
• 86 Yang C, Deng Q, Xu J. et al. Sinapic acid and resveratrol alleviate oxidative stress with modulation of gut microbiota in high-fat diet-fed rats. Food Res Int 2019; 116: 1202-1211
• 87 Buys-Gonçalves GF, Sampaio FJB, Silva MEM, Pereira-Sampaio MA, De Souza DB. Histomorphometric evaluation of the rat kidney submitted to warm ischemia and the protective effect of resveratrol. Am J Surg 2020; 220 (04) 1119-1123
• 88 Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139 (05) 871-890
• 89 Hao Q, Xiao X, Zhen J. et al. Resveratrol attenuates acute kidney injury by inhibiting death receptor–mediated apoptotic pathways in a cisplatin–induced rat model. Mol Med Rep 2016; 14 (04) 3683-3689
• 90 Chen L, Yang S, Zumbrun EE, Guan H, Nagarkatti PS, Nagarkatti M. Resveratrol attenuates lipopolysaccharide-induced acute kidney injury by suppressing inflammation driven by macrophages. Mol Nutr Food Res 2015; 59 (05) 853-864
• 91 Jang IA, Kim EN, Lim JH. et al. Effects of resveratrol on the renin-angiotensin system in the aging kidney. Nutrients 2018; 10 (11) E1741
• 92 Hong YA, Bae SY, Ahn SY. et al. Resveratrol ameliorates contrast induced nephropathy through the activation of SIRT1-PGC-1α-Foxo1 signaling in mice. Kidney Blood Press Res 2017; 42 (04) 641-653
• 93 Sabry MM, Ahmed MM, Maksoud OMA, et al. Carnitine, apelin and resveratrol regulate mitochondrial quality control (QC) related proteins and ameliorate acute kidney injury: role of hydrogen peroxide. Archives of physiology and biochemistry 2020: 1-10.
• 94 Ashrafizadeh M, Najafi M, Orouei S. et al. Resveratrol modulates transforming growth factor-beta (TGF-β) signaling pathway for disease therapy: a new insight into its pharmacological activities. Biomedicines 2020; 8 (08) E261