Recent progress in neonatal hyperoxic lung injury
Tian Rao MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Writing - original draft, Validation, Methodology, Formal analysis, Writing - review & editing
Search for more papers by this authorYiyang Zhou MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Validation, Software, Data curation, Writing - review & editing
Search for more papers by this authorChizhang Chen MSc
Department of Clinical Medicine, Chinese Medicine Hospital of Pingyang, Wenzhou, Zhejiang, China
Contribution: Investigation, Validation, Software, Data curation
Search for more papers by this authorJiayi Chen MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Validation, Data curation, Investigation, Formal analysis
Search for more papers by this authorJie Zhang MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Software, Formal analysis, Investigation, Data curation
Search for more papers by this authorCorresponding Author
Wei Lin PhD
Department of Pediatrics, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Correspondence Wei Lin, PhD, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, 325000, Zhejiang, China.
Email: [email protected]
Danyun Jia, PhD, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou 325000, Zhejiang, China.
Email: [email protected]
Contribution: Supervision, Funding acquisition, Resources, Writing - review & editing, Conceptualization
Search for more papers by this authorCorresponding Author
Danyun Jia PhD
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Correspondence Wei Lin, PhD, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, 325000, Zhejiang, China.
Email: [email protected]
Danyun Jia, PhD, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou 325000, Zhejiang, China.
Email: [email protected]
Contribution: Supervision, Resources, Funding acquisition, Conceptualization, Methodology, Formal analysis, Writing - review & editing
Search for more papers by this authorTian Rao MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Writing - original draft, Validation, Methodology, Formal analysis, Writing - review & editing
Search for more papers by this authorYiyang Zhou MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Validation, Software, Data curation, Writing - review & editing
Search for more papers by this authorChizhang Chen MSc
Department of Clinical Medicine, Chinese Medicine Hospital of Pingyang, Wenzhou, Zhejiang, China
Contribution: Investigation, Validation, Software, Data curation
Search for more papers by this authorJiayi Chen MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Validation, Data curation, Investigation, Formal analysis
Search for more papers by this authorJie Zhang MSc
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Contribution: Software, Formal analysis, Investigation, Data curation
Search for more papers by this authorCorresponding Author
Wei Lin PhD
Department of Pediatrics, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Correspondence Wei Lin, PhD, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, 325000, Zhejiang, China.
Email: [email protected]
Danyun Jia, PhD, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou 325000, Zhejiang, China.
Email: [email protected]
Contribution: Supervision, Funding acquisition, Resources, Writing - review & editing, Conceptualization
Search for more papers by this authorCorresponding Author
Danyun Jia PhD
Department of Anesthesiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, Zhejiang, China
Correspondence Wei Lin, PhD, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou, 325000, Zhejiang, China.
Email: [email protected]
Danyun Jia, PhD, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou Medical University, Wenzhou 325000, Zhejiang, China.
Email: [email protected]
Contribution: Supervision, Resources, Funding acquisition, Conceptualization, Methodology, Formal analysis, Writing - review & editing
Search for more papers by this authorTian Rao and Yiyang Zhou are co-first authors.
Abstract
With the progress in neonatal intensive care, there has been an increase in the survival rates of premature infants. However, this has also led to an increased incidence of neonatal hyperoxia lung injury and bronchopulmonary dysplasia (BPD), whose pathogenesis is believed to be influenced by various prenatal and postnatal factors, although the exact mechanisms remain unclear. Recent studies suggest that multiple mechanisms might be involved in neonatal hyperoxic lung injury and BPD, with sex also possibly playing an important role, and numerous drugs have been proposed and shown promise for improving the treatment outcomes of hyperoxic lung injury. Therefore, this paper aims to analyze and summarize sex differences in neonatal hyperoxic lung injury, potential pathogenesis and treatment progress to provide new ideas for basic and clinical research in this field.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
REFERENCES
- 1Blencowe H, Cousens S, Oestergaard MZ, et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012; 379(9832): 2162-2172.
- 2Chawanpaiboon S, Vogel JP, Moller AB, et al. Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Global Health. 2019; 7(1): e37-e46.
- 3Vogel ER, Britt RD, Trinidad MC, et al. Perinatal oxygen in the developing lung. Can J Physiol Pharmacol. 2015; 93(2): 119-127.
- 4Buczynski BW, Maduekwe ET, O'Reilly MA. The role of hyperoxia in the pathogenesis of experimental BPD. Semin Perinatol. 2013; 37(2): 69-78.
- 5Thébaud B, Goss KN, Laughon M, et al. Bronchopulmonary dysplasia. Nat Rev Dis Primers. 2019; 5(1): 78.
- 6Bancalari E, Jain D. Bronchopulmonary dysplasia: 50 years after the original description. Neonatology. 2019; 115(4): 384-391.
- 7Gilfillan M, Bhandari A, Bhandari V. Diagnosis and management of bronchopulmonary dysplasia. BMJ. 2021; 375: n1974.
- 8Scaffa A, Yao H, Oulhen N, et al. Single-cell transcriptomics reveals lasting changes in the lung cellular landscape into adulthood after neonatal hyperoxic exposure. Redox Biol. 2021; 48:102091.
- 9Willis GR, Fernandez-Gonzalez A, Anastas J, et al. Mesenchymal stromal cell exosomes ameliorate experimental bronchopulmonary dysplasia and restore lung function through macrophage immunomodulation. Am J Respir Crit Care Med. 2018; 197(1): 104-116.
- 10Mirza H, Garcia JA, Crawford E, et al. Natural history of postnatal cardiopulmonary adaptation in infants born extremely preterm and risk for death or bronchopulmonary dysplasia. J Pediatr. 2018; 198: 187-193.
- 11Bui DS, Lodge CJ, Burgess JA, et al. Childhood predictors of lung function trajectories and future COPD risk: a prospective cohort study from the first to the sixth decade of life. Lancet Respir Med. 2018; 6(7): 535-544.
- 12Davidson L, Berkelhamer S. Bronchopulmonary dysplasia: chronic lung disease of infancy and long-term pulmonary outcomes. J Clin Med. 2017; 6(1): 4.
- 13Grimm SL, Stading RE, Robertson MJ, et al. Loss of cytochrome P450 (CYP)1B1 mitigates hyperoxia response in adult mouse lung by reprogramming metabolism and translation. Redox Biol. 2023; 64:102790.
- 14Chen S, Wu Q, Zhong D, Li C, Du L. Caffeine prevents hyperoxia-induced lung injury in neonatal mice through NLRP3 inflammasome and NF-κB pathway. Respir Res. 2020; 21(1): 140.
- 15Abais JM, Xia M, Zhang Y, Boini KM, Li PL. Redox regulation of NLRP3 inflammasomes: ROS as trigger or effector? Antioxid Redox Signaling. 2015; 22(13): 1111-1129.
- 16Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014; 157(5): 1013-1022.
- 17Liao J, Kapadia VS, Brown LS, et al. The NLRP3 inflammasome is critically involved in the development of bronchopulmonary dysplasia. Nat Commun. 2015; 6: 8977.
- 18Eitel J, Meixenberger K, van Laak C, et al. Rac1 regulates the NLRP3 inflammasome which mediates IL-1beta production in Chlamydophila pneumoniae infected human mononuclear cells. PLoS One. 2012; 7(1):e30379.
- 19Hummler JK, Dapaah-siakwan F, Vaidya R, et al. Inhibition of Rac1 signaling downregulates inflammasome activation and attenuates lung injury in neonatal rats exposed to hyperoxia. Neonatology. 2017; 111(3): 280-288.
- 20Zhang Q, Wu D, Yang Y, Liu T, Liu H. Dexmedetomidine alleviates hyperoxia-induced acute lung injury via inhibiting NLRP3 inflammasome activation. Cell Physiol Biochem. 2017; 42(5): 1907-1919.
- 21Zhang Q, Ran X, He Y, Ai Q, Shi Y. Acetate downregulates the activation of NLRP3 inflammasomes and attenuates lung injury in neonatal mice with bronchopulmonary dysplasia. Front Pediatr. 2021; 8:595157.
- 22He W, Wan H, Hu L, et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 2015; 25(12): 1285-1298.
- 23Huang Y, Xu W, Zhou R. NLRP3 inflammasome activation and cell death. Cell Mol Immunol. 2021; 18(9): 2114-2127.
- 24Sonny S, Yuan H, Chen S, et al. GSDMD deficiency ameliorates hyperoxia-induced BPD and ROP in neonatal mice. Sci Rep. 2023; 13(1): 143.
- 25Dapaah-Siakwan F, Zambrano R, Luo S, et al. Caspase-1 inhibition attenuates hyperoxia-induced lung and brain injury in neonatal mice. Am J Respir Cell Mol Biol. 2019; 61(3): 341-354.
- 26Datta A, Kim GA, Taylor JM, et al. Mouse lung development and NOX1 induction during hyperoxia are developmentally regulated and mitochondrial ROS dependent. Am J Physiol Lung Cell Mol Physiol. 2015; 309(4): L369-L377.
- 27Robbins ME, Cho HY, Hansen JM, et al. Glutathione reductase deficiency alters lung development and hyperoxic responses in neonatal mice. Redox Biol. 2021; 38:101797.
- 28Li X, Zhang B, Yan C, et al. A fast and specific fluorescent probe for thioredoxin reductase that works via disulphide bond cleavage. Nat Commun. 2019; 10(1): 2745.
- 29Li Q, Wall SB, Ren C, et al. Thioredoxin reductase inhibition attenuates neonatal hyperoxic lung injury and enhances nuclear factor E2–related factor 2 activation. Am J Respir Cell Mol Biol. 2016; 55(3): 419-428.
- 30Dunigan K, Li Q, Li R, Locy ML, Wall S, Tipple TE. The thioredoxin reductase inhibitor auranofin induces heme oxygenase-1 in lung epithelial cells via Nrf2-dependent mechanisms. Am J Physiol Lung Cell Mol Physiol. 2018; 315(4): L545-L552.
- 31Wall SB, Wood R, Dunigan K, et al. Thioredoxin reductase-1 inhibition augments endogenous glutathione-dependent antioxidant responses in experimental bronchopulmonary dysplasia. Oxid Med Cell Longevity. 2019; 2019: 1-10.
- 32Ozdemir R, Gokce IK, Taslidere AC, et al. Does Chrysin prevent severe lung damage in Hyperoxia-Induced lung injury Model? Int Immunopharmacol. 2021; 99:108033.
- 33Tayman C, Çakır U, Akduman H, Karabulut Ş, Çağlayan M. The therapeutic effect of Apocynin against hyperoxy and Inflammation-Induced lung injury. Int Immunopharmacol. 2021; 101(Pt A):108190.
- 34Lavoie JC, Mohamed I, Teixeira V. Dose–response effects of glutathione supplement in parenteral nutrition on pulmonary oxidative stress and alveolarization in newborn guinea pig. Antioxidants. 2022; 11(10): 1956.
- 35Jia D, Zheng J, Zhou Y, et al. Ferroptosis is involved in hyperoxic lung injury in neonatal rats. J Inflamm Res. 2021; 14: 5393-5401.
- 36Amata E, Pittalà V, Marrazzo A, et al. Role of the Nrf2/HO-1 axis in bronchopulmonary dysplasia and hyperoxic lung injuries. Clin Sci. 2017; 131(14): 1701-1712.
- 37Stading R, Chu C, Couroucli X, Lingappan K, Moorthy B. Molecular role of cytochrome P4501A enzymes inoxidative stress. Curr Opin Toxicol. 2020; 20-21: 77-84.
- 38Gao F, Li C, Smith SM, et al. Decoding the IGF1 signaling gene regulatory network behind alveologenesis from a mouse model of bronchopulmonary dysplasia. eLife. 2022; 11:e77522.
- 39Huang L, Guo N, Cheng M, Wang J, Chen F, Shi Y. The value of plasma insulin-like growth factor 1 and interleukin-18 in the diagnosis of bronchopulmonary dysplasia in premature infants. Front Pediatr. 2022; 10:1013537.
- 40Seedorf G, Kim C, Wallace B, et al. rhIGF-1/BP3 preserves lung growth and prevents pulmonary hypertension in experimental bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2020; 201(9): 1120-1134.
- 41Albertine KH, Dahl MJ, Rebentisch A, et al. Pilot dose-ranging of rhIGF-1/rhIGFBP-3 in a preterm lamb model of evolving bronchopulmonary dysplasia. Pediatr Res. 2022; 93: 1528-1538.
- 42Sun X, Perl AK, Li R, et al. A census of the lung: CellCards from LungMAP. Dev Cell. 2022; 57(1): 112-145.
- 43Vohlen C, Mohr J, Fomenko A, et al. Dynamic regulation of GH–IGF1 signaling in injury and recovery in hyperoxia-induced neonatal lung injury. Cells. 2021; 10(11): 2947.
- 44Chao CM, Carraro G, Rako ZA, et al. Failure to down-regulate miR-154 expression in early postnatal mouse lung epithelium suppresses alveologenesis, with changes in Tgf-β signaling similar to those induced by exposure to hyperoxia. Cells. 2020; 9(4): 859.
- 45Gong J, Feng Z, Peterson AL, et al. Endothelial to mesenchymal transition during neonatal hyperoxia-induced pulmonary hypertension. J Pathol. 2020; 252(4): 411-422.
- 46Jin M, Lee J, Lee K, Jin Z, Pak JH, Kim HS. Alteration of TGF-β-ALK-Smad signaling in hyperoxia-induced bronchopulmonary dysplasia model of newborn rats. Exp Lung Res. 2016; 42(7): 354-364.
- 47Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136(2): 215-233.
- 48Alam MA, Betal SG, Aghai ZH, Bhandari V. Hyperoxia causes miR199a-5p-mediated injury in the developing lung. Pediatr Res. 2019; 86(5): 579-588.
- 49Freeman A, Qiao L, Olave N, et al. MicroRNA 219-5p inhibits alveolarization by reducing platelet derived growth factor receptor-alpha. Respir Res. 2021; 22(1): 57.
- 50Zhang ZQ, Hong H, Li J, Li XX, Huang XM. MicroRNA-214 promotes alveolarization in neonatal rat models of bronchopulmonary dysplasia via the PlGF-dependent STAT3 pathway. Mol Med. 2021; 27(1): 109.
- 51Hu Y, Xie L, Yu J, Fu H, Zhou D, Liu H. Inhibition of microRNA-29a alleviates hyperoxia-induced bronchopulmonary dysplasia in neonatal mice via upregulation of GAB1. Mol Med. 2019; 26(1): 3.
- 52Wen X, Zhang H, Xiang B, et al. Hyperoxia-induced miR-342-5p down-regulation exacerbates neonatal bronchopulmonary dysplasia via the Raf1 regulator Spred3. Br J Pharmacol. 2021; 178(11): 2266-2283.
- 53Rogers LK, Robbins M, Dakhlallah D, et al. Attenuation of miR-17∼92 cluster in bronchopulmonary dysplasia. Ann Am Thorac Soc. 2015; 12(10): 1506-1513.
- 54Robbins ME, Dakhlallah D, Marsh CB, Rogers LK, Tipple TE. Of mice and men: correlations between microRNA-17∼92 cluster expression and promoter methylation in severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2016; 311(5): L981-L984.
- 55Schmitz SU, Grote P, Herrmann BG. Mechanisms of long noncoding RNA function in development and disease. Cell Mol Life Sci. 2016; 73(13): 2491-2509.
- 56Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell. 2011; 146(3): 353-358.
- 57Wang J, Yin J, Wang X, et al. Changing expression profiles of mRNA, lncRNA, circRNA, and miRNA in lung tissue reveal the pathophysiological of bronchopulmonary dysplasia (BPD) in mouse model. J Cell Biochem. 2019; 120(6): 9369-9380.
- 58Zou DM, Zhou SM, Li LH, Zhou JL, Tang ZM, Wang SH. Knockdown of long noncoding RNAs of maternally expressed 3 alleviates hyperoxia-induced lung injury via inhibiting thioredoxin-interacting protein–mediated pyroptosis by binding to miR-18a. Am J Pathol. 2020; 190(5): 994-1005.
- 59Tipple TE, Welty SE, Nelin LD, Hansen JM, Rogers LK. Alterations of the thioredoxin system by hyperoxia: implications for alveolar development. Am J Respir Cell Mol Biol. 2009; 41(5): 612-619.
- 60Zhang L, Wang P, Shen Y, Huang T, Hu X, Yu W. Mechanism of lncRNA H19 in regulating pulmonary injury in hyperoxia-induced bronchopulmonary dysplasia newborn mice. Am J Perinatol. 2022; 39(10): 1089-1096.
- 61Mo W, Li Y, Chang W, Luo Y, Mai B, Zhou J. The role of LncRNA H19 in MAPK signaling pathway implicated in the progression of bronchopulmonary dysplasia. Cell Transplant. 2020; 29:096368972091829.
- 62Wang Y, Wang X, Xu Q, Yin J, Wang H, Zhang L. CircRNA, lncRNA, and mRNA profiles of umbilical cord blood exosomes from preterm newborns showing bronchopulmonary dysplasia. Eur J Pediatr. 2022; 181(9): 3345-3365.
- 63Cai C, Qiu J, Qiu G, et al. Long non-coding RNA MALAT1 protects preterm infants with bronchopulmonary dysplasia by inhibiting cell apoptosis. BMC Pulm Med. 2017; 17(1): 199.
- 64Zhao X, Shi Y, Zhang D, et al. Autophagy inducer activates Nrf2-ARE pathway to attenuate aberrant alveolarization in neonatal rats with bronchopulmonary dysplasia. Life Sci. 2020; 252:117662.
- 65Teng RJ, Jing X, Martin DP, et al. N-acetyl-lysyltyrosylcysteine amide, a novel systems pharmacology agent, reduces bronchopulmonary dysplasia in hyperoxic neonatal rat pups. Free Radic Biol Med. 2021; 166: 73-89.
- 66Li J, Shi J, Li P, Guo X, Wang T, Liu A. Genipin attenuates hyperoxia-induced lung injury and pulmonary hypertension via targeting glycogen synthase kinase-3 β in neonatal rats. Nutrition. 2019; 57: 237-244.
- 67Lamorte S, Shinde R, McGaha TL. Nuclear receptors, the aryl hydrocarbon receptor, and macrophage function. Mol Aspects Med. 2021; 78:100942.
- 68Maturu P, Wei-Liang Y, Jiang W, et al. Newborn mice lacking the gene for Cyp1a1 are more susceptible to oxygen-mediated lung injury, and are rescued by postnatal β-naphthoflavone administration: implications for bronchopulmonary dysplasia in premature infants. Toxicol Sci. 2017; 157(1): 260-271.
- 69Lingappan K, Maturu P, Liang YW, et al. β-Naphthoflavone treatment attenuates neonatal hyperoxic lung injury in wild type and Cyp1a2-knockout mice. Toxicol Appl Pharmacol. 2018; 339: 133-142.
- 70Chen JH, Feng DD, Chen YF, et al. Long non-coding RNA MALAT1 targeting STING transcription promotes bronchopulmonary dysplasia through regulation of CREB. J Cell Mol Med. 2020; 24(18): 10478-10492.
- 71Bolte C, Ustiyan V, Ren X, et al. Nanoparticle delivery of proangiogenic transcription factors into the neonatal circulation inhibits alveolar simplification caused by hyperoxia. Am J Respir Crit Care Med. 2020; 202(1): 100-111.
- 72Ashley SL, Sjoding MW, Popova AP, et al. Lung and gut microbiota are altered by hyperoxia and contribute to oxygen-induced lung injury in mice. Sci Transl Med. 2020; 12(556):eaau9959.
- 73Dolma K, Freeman AE, Rezonzew G, et al. Effects of hyperoxia on alveolar and pulmonary vascular development in germ-free mice. Am J Physiol Lung Cell Mol Physiol. 2020; 318(2): L421-L428.
- 74Chen CM, Chou HC, Yang YCSH, Su ECY, Liu YR. Predicting hyperoxia-induced lung injury from associated intestinal and lung dysbiosis in neonatal mice. Neonatology. 2021; 118(2): 163-173.
- 75Chen CM, Yang YCSH, Chou HC. Maternal antibiotic exposure disrupts microbiota and exacerbates hyperoxia-induced lung injury in neonatal mice. Pediatr Res. 2021; 90(4): 776-783.
- 76Gentle SJ, Lal CV. Predicting BPD: lessons learned from the airway microbiome of preterm infants. Front Pediatr. 2020; 7: 564.
- 77Tirone C, Pezza L, Paladini A, et al. Gut and lung microbiota in preterm infants: immunological modulation and implication in neonatal outcomes. Front Immunol. 2019; 10: 2910.
- 78Ryan FJ, Drew DP, Douglas C, et al. Changes in the composition of the gut microbiota and the blood transcriptome in preterm infants at less than 29 weeks gestation diagnosed with bronchopulmonary dysplasia. mSystems. 2019; 4(5):10-1128.
- 79Capasso L, Vento G, Loddo C, et al. Oxidative stress and bronchopulmonary dysplasia: evidences from microbiomics, metabolomics, and proteomics. Front Pediatr. 2019; 7: 30.
- 80Li Y, He L, Zhao Q, Bo T. Microbial and metabolic profiles of bronchopulmonary dysplasia and therapeutic effects of potential probiotics Limosilactobacillus reuteri and Bifidobacterium bifidum. J Appl Microbiol. 2022; 133(2): 908-921.
- 81Lai PY, Jing X, Michalkiewicz T, et al. Adverse early-life environment impairs postnatal lung development in mice. Physiol Genomics. 2019; 51(9): 462-470.
- 82Diniz MS, Magalhães CC, Tocantins C, Grilo LF, Teixeira J, Pereira SP. Nurturing through nutrition: exploring the role of antioxidants in maternal diet during pregnancy to mitigate developmental programming of chronic diseases. Nutrients. 2023; 15(21): 4623.
- 83Chen H, Zhang W, Sun X, et al. Prenatal exposure to multiple environmental chemicals and birth size. J Exposure Sci Environ Epidemiol. Published online July 08, 2023. doi:10.1038/s41370-023-00568-4
- 84Gómez-Roig MD, Pascal R, Cahuana MJ, et al. Environmental exposure during pregnancy: influence on prenatal development and early life: a comprehensive review. Fetal Diagn Ther. 2021; 48(4): 245-257.
- 85Coarfa C, Grimm SL, Katz T, et al. Epigenetic response to hyperoxia in the neonatal lung is sexually dimorphic. Redox Biol. 2020; 37:101718.
- 86Grimm SL, Dong X, Zhang Y, et al. Effect of sex chromosomes versus hormones in neonatal lung injury. JCI Insight. 2021; 6(13):e146863.
- 87Lingappan K, Jiang W, Wang L, Moorthy B. Sex-specific differences in neonatal hyperoxic lung injury. Am J Physiol Lung Cell Mol Physiol. 2016; 311(2): L481-L493.
- 88Hammond 2nd, JD, Kielt MJ, Conroy S, et al. Exploring the association of male sex with adverse outcomes in severe bronchopulmonary dysplasia: a retrospective, multicenter cohort study. Chest. 2024; 165(3): 610-620.
- 89Tondreau MY, Boucher E, Simard M, Tremblay Y, Bilodeau JF. Sex-specific perinatal expression of glutathione peroxidases during mouse lung development. Mol Cell Endocrinol. 2012; 355(1): 87-95.
- 90Zhang Y, Lingappan K. Differential sex-specific effects of oxygen toxicity in human umbilical vein endothelial cells. Biochem Biophys Res Commun. 2017; 486(2): 431-437.
- 91Han ES, Muller FL, Pérez VI, et al. The in vivo gene expression signature of oxidative stress. Physiol Genomics. 2008; 34(1): 112-126.
- 92Clark BJ, Bull TM, Benson AB, et al. Growth differentiation factor-15 and prognosis in acute respiratory distress syndrome: a retrospective cohort study. Crit Care. 2013; 17(3): R92.
- 93Kempf T, Wollert KC. Risk stratification in critically ill patients: GDF-15 scores in adult respiratory distress syndrome. Crit Care. 2013; 17(4): 173.
- 94Zhang Y, Jiang W, Wang L, Lingappan K. Sex-specific differences in the modulation of growth differentiation factor 15 (GDF15) by hyperoxia in vivo and in vitro: role of Hif-1α. Toxicol Appl Pharmacol. 2017; 332: 8-14.
- 95Mammoto A, Mammoto T. Vascular niche in lung alveolar development, homeostasis, and regeneration. Front Bioeng Biotechnol. 2019; 7: 318.
- 96Coarfa C, Zhang Y, Maity S, et al. Sexual dimorphism of the pulmonary transcriptome in neonatal hyperoxic lung injury: identification of angiogenesis as a key pathway. Am J Physiol Lung Cell Mol Physiol. 2017; 313(6): L991-L1005.
- 97Choi CW, Lee J, Lee HJ, Park HS, Chun YS, Kim BI. Deferoxamine improves alveolar and pulmonary vascular development by upregulating hypoxia-inducible factor-1α in a rat model of bronchopulmonary dysplasia. J Korean Med Sci. 2015; 30(9): 1295-1301.
- 98Compernolle V, Brusselmans K, Acker T, et al. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nature Med. 2002; 8(7): 702-710.
- 99Hellström M, Phng LK, Hofmann JJ, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007; 445(7129): 776-780.
- 100Murinello S, Usui Y, Sakimoto S, et al. miR-30a-5p inhibition promotes interaction of Fas(+) endothelial cells and FasL(+) microglia to decrease pathological neovascularization and promote physiological angiogenesis. GLIA. 2019; 67(2): 332-344.
- 101Zhang Y, Coarfa C, Dong X, et al. MicroRNA-30a as a candidate underlying sex-specific differences in neonatal hyperoxic lung injury: implications for BPD. Am J Physiol Lung Cell Mol Physiol. 2019; 316(1): L144-L156.
- 102Zhang Y, Dong X, Lingappan K. Role of HIF-1α-miR30a-Snai1 axis in neonatal hyperoxic lung injury. Oxid Med Cell Longev. 2019; 2019:8327486.
- 103Cantu A, Cantu Gutierrez M, Zhang Y, Dong X, Lingappan K. Endothelial to mesenchymal transition in neonatal hyperoxic lung injury: role of sex as a biological variable. Physiol Genomics. 2023; 55(8): 345-354.
- 104Pitulescu ME, Schmidt I, Giaimo BD, et al. Dll4 and Notch signalling couples sprouting angiogenesis and artery formation. Nature Cell Biol. 2017; 19(8): 915-927.
- 105Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016; 32(1): 42-56.
- 106McGrath-Morrow SA, Cho C, Soutiere S, Mitzner W, Tuder R. The effect of neonatal hyperoxia on the lung of p21Waf1/Cip1/Sdi1-deficient mice. Am J Respir Cell Mol Biol. 2004; 30(5): 635-640.
- 107Rama N, Dubrac A, Mathivet T, et al. Slit2 signaling through Robo1 and Robo2 is required for retinal neovascularization. Nature Med. 2015; 21(5): 483-491.
- 108Pilling D, Zheng Z, Vakil V, Gomer RH. Fibroblasts secrete Slit2 to inhibit fibrocyte differentiation and fibrosis. Proc Natl Acad Sci USA. 2014; 111(51): 18291-18296.
- 109Milianti FJ, Cullinan WL. Effects of age and word frequency on object recognition and naming in children. J Speech Hear Res. 1974; 17(3): 373-385.
- 110Chen NY, D. Collum S, Luo F, et al. Macrophage bone morphogenic protein receptor 2 depletion in idiopathic pulmonary fibrosis and Group III pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2016; 311(2): L238-L254.
- 111Abman SH, Bancalari E, Jobe A. The evolution of bronchopulmonary dysplasia after 50 years. Am J Respir Crit Care Med. 2017; 195(4): 421-424.
- 112Chang YS, Ahn SY, Jeon HB, et al. Critical role of vascular endothelial growth factor secreted by mesenchymal stem cells in hyperoxic lung injury. Am J Respir Cell Mol Biol. 2014; 51(3): 391-399.
- 113Kwon JH, Kim M, Bae YK, et al. Decorin secreted by human umbilical cord blood-derived mesenchymal stem cells induces macrophage polarization via CD44 to repair hyperoxic lung injury. Int J Mol Sci. 2019; 20(19): 4815.
- 114Kim M, Kwon JH, Bae YK, et al. Soluble PTX3 of human umbilical cord blood-derived mesenchymal stem cells attenuates hyperoxic lung injury by activating macrophage polarization in neonatal rat model. Stem Cells Int. 2020; 2020: 1-18.
- 115Clement A, Chadelat K, Sardet A, Grimfeld A, Tournier G. Alveolar macrophage status in bronchopulmonary dysplasia. Pediatr Res. 1988; 23(5): 470-473.
- 116Nold MF, Mangan NE, Rudloff I, et al. Interleukin-1 receptor antagonist prevents murine bronchopulmonary dysplasia induced by perinatal inflammation and hyperoxia. Proc Natl Acad Sci USA. 2013; 110(35): 14384-14389.
- 117Bui CB, Kolodziej M, Lamanna E, et al. Interleukin-1 receptor antagonist protects newborn mice against pulmonary hypertension. Front Immunol. 2019; 10: 1480.
- 118Dumpa V, Nielsen L, Wang H, Kumar VHS. Caffeine is associated with improved alveolarization and angiogenesis in male mice following hyperoxia induced lung injury. BMC Pulm Med. 2019; 19(1): 138.
- 119Pritchard Jr., KA, X, Jing, Teng M, et al. Role of endoplasmic reticulum stress in impaired neonatal lung growth and bronchopulmonary dysplasia. PLoS One. 2022; 17(8):e0269564.
- 120Wang Y, Jiang L. Role of vitamin D-vitamin D receptor signaling on hyperoxia-induced bronchopulmonary dysplasia in neonatal rats. Pediatr Pulmonol. 2021; 56(7): 2335-2344.
- 121Park HW, Lim G, Park YM, Chang M, Son JS, Lee R. Association between vitamin D level and bronchopulmonary dysplasia: a systematic review and meta-analysis. PLoS One. 2020; 15(7):e0235332.
- 122Ge H, Liu W, Li H, et al. The association of vitamin D and vitamin E levels at birth with bronchopulmonary dysplasia in preterm infants. Pediatr Pulmonol. 2021; 56(7): 2108-2113.
- 123Williams AR, Hare JM. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res. 2011; 109(8): 923-940.
- 124Porzionato A, Zaramella P, Dedja A, et al. Intratracheal administration of clinical-grade mesenchymal stem cell-derived extracellular vesicles reduces lung injury in a rat model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2019; 316(1): L6-L19.
- 125Mei Y, Chen C, Dong H, et al. Treatment of hyperoxia-induced lung injury with lung mesenchymal stem cells in mice. Stem Cells Int. 2018; 2018: 1-8.
- 126Thébaud B, Ladha F, Michelakis ED, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia-induced lung injury: evidence that angiogenesis participates in alveolarization. Circulation. 2005; 112(16): 2477-2486.
- 127Ahn SY, Park WS, Kim YE, et al. Vascular endothelial growth factor mediates the therapeutic efficacy of mesenchymal stem cell-derived extracellular vesicles against neonatal hyperoxic lung injury. Exp Mol Med. 2018; 50(4): 1-12.
- 128Porzionato A, Zaramella P, Dedja A, et al. Intratracheal administration of mesenchymal stem cell-derived extracellular vesicles reduces lung injuries in a chronic rat model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2021; 320(5): L688-L704.
- 129Sharma M, Bellio MA, Benny M, et al. Mesenchymal stem cell-derived extracellular vesicles prevent experimental bronchopulmonary dysplasia complicated by pulmonary hypertension. Stem Cells Transl Med. 2022; 11(8): 828-840.
- 130Chang YS, Ahn SY, Yoo HS, et al. Mesenchymal stem cells for bronchopulmonary dysplasia: phase 1 dose-escalation clinical trial. J Pediatr. 2014; 164(5): 966-972.
- 131Ahn SY, Chang YS, Kim JH, Sung SI, Park WS. Two-year follow-up outcomes of premature infants enrolled in the phase I trial of mesenchymal stem cells transplantation for bronchopulmonary dysplasia. J Pediatr. 2017; 185: 49-54.
- 132Ahn SY, Chang YS, Lee MH, et al. Stem cells for bronchopulmonary dysplasia in preterm infants: a randomized controlled phase II trial. Stem Cells Transl Med. 2021; 10(8): 1129-1137.
- 133Walsh MC, Szefler S, Davis J, et al. Summary proceedings from the bronchopulmonary dysplasia group. Pediatrics. 2006; 117(3 Pt 2): S52-S56.
- 134McEvoy CT, Jain L, Schmidt B, Abman S, Bancalari E, Aschner JL. Bronchopulmonary dysplasia: NHLBI workshop on the primary prevention of chronic lung diseases. Ann Am Thorac Soc. 2014; 11(suppl 3): S146-S153.
- 135Trankle CR, Canada JM, Kadariya D, et al. IL-1 blockade reduces inflammation in pulmonary arterial hypertension and right ventricular failure: a single-arm, open-label, phase IB/II pilot study. Am J Respir Crit Care Med. 2019; 199(3): 381-384.
- 136Royce SG, Nold MF, Bui C, et al. Airway remodeling and hyperreactivity in a model of bronchopulmonary dysplasia and their modulation by IL-1 receptor antagonist. Am J Respir Cell Mol Biol. 2016; 55(6): 858-868.
- 137Green EA, Metz D, Galinsky R, et al. Anakinra Pilot - a clinical trial to demonstrate safety, feasibility and pharmacokinetics of interleukin 1 receptor antagonist in preterm infants. Front Immunol. 2022; 13:1022104.
- 138Hirani D, Alvira CM, Danopoulos S, et al. Macrophage-derived IL-6 trans-signalling as a novel target in the pathogenesis of bronchopulmonary dysplasia. Eur Respir J. 2022; 59(2):2002248.
- 139Gao R, Li Z, Ai D, Ma J, Chen C, Liu X. Interleukin-24 as a pulmonary target cytokine in bronchopulmonary dysplasia. Cell Biochem Biophys. 2021; 79(2): 311-320.
- 140Jin R, Xu J, Gao Q, et al. IL-33-induced neutrophil extracellular traps degrade fibronectin in a murine model of bronchopulmonary dysplasia. Cell Death Discov. 2020; 6: 33.
- 141Jobe AH. Caffeine: a lung drug for all very low birth weight preterm infants? Am J Respir Crit Care Med. 2017; 196(10): 1241-1243.
- 142Endesfelder S, Strauß E, Bendix I, Schmitz T, Bührer C. Prevention of oxygen-induced inflammatory lung injury by caffeine in neonatal rats. Oxid Med Cell Longevity. 2020; 2020: 1-19.
- 143Zhang H, Jing X, Shi Y, et al. N-acetyl lysyltyrosylcysteine amide inhibits myeloperoxidase, a novel tripeptide inhibitor. J Lipid Res. 2013; 54(11): 3016-3029.
- 144Zhen H, Hu H, Rong G, Huang X, Tan C, Yu X. VitA or VitD ameliorates bronchopulmonary dysplasia by regulating the balance between M1 and M2 macrophages. Biomed Pharmacother. 2021; 141:111836.
- 145Hu J, Wu Z, Wang H, et al. Vitamin D ameliorates apoptosis and inflammation by targeting the mitochondrial and MEK1/2-ERK1/2 pathways in hyperoxia-induced bronchopulmonary dysplasia. J Inflamm Res. 2022; 15: 4891-4906.
- 146Yao L, Shi Y, Zhao X, et al. Vitamin D attenuates hyperoxia-induced lung injury through downregulation of Toll-like receptor 4. Int J Mol Med. 2017; 39(6): 1403-1408.
- 147Doyle LW, Cheong JL, Hay S, Manley BJ, Halliday HL. Early (<7 days) systemic postnatal corticosteroids for prevention of bronchopulmonary dysplasia in preterm infants. Cochrane Database Syst Rev. 2021; 11(11):001145.
- 148Özer Bekmez B, Tayman C, Çakır U, et al. Glucocorticoids in a neonatal hyperoxic lung injury model: pulmonary and neurotoxic effects. Pediatr Res. 2022; 92(2): 436-444.
- 149Abiramalatha T, Ramaswamy VV, Bandyopadhyay T, et al. Interventions to prevent bronchopulmonary dysplasia in preterm neonates: an umbrella review of systematic reviews and meta-analyses. JAMA Pediatr. 2022; 176(5): 502-516.
- 150Wang H, Yan D, Wu Z, Geng H, Zhu X, Zhu X. Predictive values of clinical data,molecular biomarkers, and echocardiographic measurements in preterm infants with bronchopulmonary dysplasia. Front Pediatr. 2023; 10:1070858.
- 151Euteneuer JC, Kerns E, Leiting C, McCulloh RJ, Peeples ES. Inhaled bronchodilator exposure in the management of bronchopulmonary dysplasia in hospitalized infants. J Perinatol. 2021; 41(1): 53-61.
- 152Williams E, Greenough A. Advances in treating bronchopulmonary dysplasia. Expert Rev Respir Med. 2019; 13(8): 727-735.