View Item 

Show simple item record

Human induced pluripotent stem cell‐derived lung organoids in an ex vivo model of the congenital diaphragmatic hernia fetal lung

dc.contributor.authorKunisaki, Shaun M.
dc.contributor.authorJiang, Guihua
dc.contributor.authorBiancotti, Juan C.
dc.contributor.authorHo, Kenneth K. Y.
dc.contributor.authorDye, Briana R.
dc.contributor.authorLiu, Allen P.
dc.contributor.authorSpence, Jason R.
dc.date.accessioned2021-01-05T18:44:27Z
dc.date.availableWITHHELD_13_MONTHS
dc.date.available2021-01-05T18:44:27Z
dc.date.issued2021-01
dc.identifier.citationKunisaki, Shaun M.; Jiang, Guihua; Biancotti, Juan C.; Ho, Kenneth K. Y.; Dye, Briana R.; Liu, Allen P.; Spence, Jason R. (2021). "Human induced pluripotent stem cell‐derived lung organoids in an ex vivo model of the congenital diaphragmatic hernia fetal lung." STEM CELLS Translational Medicine 10(1): 98-114.
dc.identifier.issn2157-6564
dc.identifier.issn2157-6580
dc.identifier.urihttps://hdl.handle.net/2027.42/163782
dc.description.abstractThree‐dimensional lung organoids (LOs) derived from pluripotent stem cells have the potential to enhance our understanding of disease mechanisms and to enable novel therapeutic approaches in neonates with pulmonary disorders. We established a reproducible ex vivo model of lung development using transgene‐free human induced pluripotent stem cells generated from fetuses and infants with Bochdalek congenital diaphragmatic hernia (CDH), a polygenic disorder associated with fetal lung compression and pulmonary hypoplasia at birth. Molecular and cellular comparisons of CDH LOs revealed impaired generation of NKX2.1+ progenitors, type II alveolar epithelial cells, and PDGFRα+ myofibroblasts. We then subjected these LOs to disease relevant mechanical cues through ex vivo compression and observed significant changes in genes associated with pulmonary progenitors, alveolar epithelial cells, and mesenchymal fibroblasts. Collectively, these data suggest both primary cell‐intrinsic and secondary mechanical causes of CDH lung hypoplasia and support the use of this stem cell‐based approach for disease modeling in CDH.We established a reproducible ex vivo model of lung development using transgene‐free human induced pluripotent stem cells generated from fetuses and infants with Bochdalek congenital diaphragmatic hernia (CDH). Both primary cell‐intrinsic and secondary causes of CDH lung hypoplasia were identified, and mechanical compression was associated with alterations in lung organoid epithelial and mesenchymal gene regulation.
dc.publisherJohn Wiley & Sons, Inc.
dc.subject.otherfetal lung
dc.subject.otherinduced pluripotent stem cells
dc.subject.otherlung organoids
dc.subject.othermechanical compression
dc.subject.othercongenital diaphragmatic hernia
dc.titleHuman induced pluripotent stem cell‐derived lung organoids in an ex vivo model of the congenital diaphragmatic hernia fetal lung
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/163782/1/sct312826.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/163782/2/sct312826_am.pdf
dc.identifier.doi10.1002/sctm.20-0199
dc.identifier.sourceSTEM CELLS Translational Medicine
dc.identifier.citedreferenceClugston RD, Zhang W, Greer JJ. Gene expression in the developing diaphragm: significance for congenital diaphragmatic hernia. Am J Physiol Lung Cell Mol Physiol. 2008; 294: L665 ‐ L675.
dc.identifier.citedreferenceMolenaar JC, Bos AP, Hazebroek FW, et al. Congenital diaphragmatic hernia, what defect? J Pediatr Surg. 1991; 26: 248 ‐ 254.
dc.identifier.citedreferenceFeatherstone NC, Connell MG, Fernig DG, et al. Airway smooth muscle dysfunction precedes teratogenic congenital diaphragmatic hernia and may contribute to hypoplastic lung morphogenesis. Am J Respir Cell Mol Biol. 2006; 35: 571 ‐ 578.
dc.identifier.citedreferenceMontalva L, Zani A. Assessment of the nitrofen model of congenital diaphragmatic hernia and of the dysregulated factors involved in pulmonary hypoplasia. Pediatr Surg Int. 2019; 35: 41 ‐ 61.
dc.identifier.citedreferenceDi Bernardo J, Maiden MM, Hershenson MB, et al. Amniotic fluid derived mesenchymal stromal cells augment fetal lung growth in a nitrofen explant model. J Pediatr Surg. 2014; 49: 859 ‐ 865.
dc.identifier.citedreferenceLeinwand MJ, Tefft JD, Zhao J, Coleman C, Anderson KD, Warburton D. Nitrofen inhibition of pulmonary growth and development occurs in the early embryonic mouse. J Pediatr Surg. 2002; 37: 1263 ‐ 1268.
dc.identifier.citedreferencevan Loenhout RB, Tseu I, Fox EK, et al. The pulmonary mesenchymal tissue layer is defective in an in vitro recombinant model of nitrofen‐induced lung hypoplasia. Am J Pathol. 2012; 180: 48 ‐ 60.
dc.identifier.citedreferenceCostlow RD, Manson JM. The heart and diaphragm: target organs in the neonatal death induced by nitrofen (2,4‐dichlorophenyl‐p‐nitrophenyl ether). Toxicology. 1981; 20: 209 ‐ 227.
dc.identifier.citedreferenceDonahoe PK, Longoni M, High FA. Polygenic causes of congenital diaphragmatic hernia produce common lung pathologies. Am J Pathol. 2016; 186: 2532 ‐ 2543.
dc.identifier.citedreferenceLeeman KT, Pessina P, Lee JH, Kim CF. Mesenchymal stem cells increase alveolar differentiation in lung progenitor organoid cultures. Sci Rep. 2019; 9: 6479.
dc.identifier.citedreferenceDeimling J, Thompson K, Tseu I, et al. Mesenchymal maintenance of distal epithelial cell phenotype during late fetal lung development. Am J Physiol Lung Cell Mol Physiol. 2007; 292: L725 ‐ L741.
dc.identifier.citedreferenceKotecha S. Lung growth: implications for the newborn infant. Arch Dis Child Fetal Neonatal Ed. 2000; 82: F69 ‐ F74.
dc.identifier.citedreferenceColeman C, Zhao J, Gupta M, et al. Inhibition of vascular and epithelial differentiation in murine nitrofen‐induced diaphragmatic hernia. Am J Physiol. 1998; 274: L636 ‐ L646.
dc.identifier.citedreferenceSluiter I, van der Horst I, van der Voorn P, et al. Premature differentiation of vascular smooth muscle cells in human congenital diaphragmatic hernia. Exp Mol Pathol. 2013; 94: 195 ‐ 202.
dc.identifier.citedreferenceUnger S, Copland I, Tibboel D, Post M. Down‐regulation of sonic hedgehog expression in pulmonary hypoplasia is associated with congenital diaphragmatic hernia. Am J Pathol. 2003; 162: 547 ‐ 555.
dc.identifier.citedreferenceBougault C, Paumier A, Aubert‐Foucher E, Mallein‐Gerin F. Molecular analysis of chondrocytes cultured in agarose in response to dynamic compression. BMC Biotechnol. 2008; 8: 71.
dc.identifier.citedreferenceMiller AJ, Hill DR, Nagy MS, et al. In vitro induction and in vivo engraftment of lung bud tip progenitor cells derived from human pluripotent stem cells. Stem Cell Reports. 2018; 10: 101 ‐ 119.
dc.identifier.citedreferenceChen YW, Huang SX, de Carvalho A, et al. A three‐dimensional model of human lung development and disease from pluripotent stem cells. Nat Cell Biol. 2017; 19: 542 ‐ 549.
dc.identifier.citedreferenceLeibel SL, Winquist A, Tseu I, et al. Reversal of surfactant protein B deficiency in patient specific human induced pluripotent stem cell derived lung organoids by gene therapy. Sci Rep. 2019; 9: 13450.
dc.identifier.citedreferencePieretti AC, Ahmed AM, Roberts JD Jr, et al. A novel in vitro model to study alveologenesis. Am J Respir Cell Mol Biol. 2014; 50: 459 ‐ 469.
dc.identifier.citedreferenceMuehlethaler V, Kunig AM, Seedorf G, Balasubramaniam V, Abman SH. Impaired VEGF and nitric oxide signaling after nitrofen exposure in rat fetal lung explants. Am J Physiol Lung Cell Mol Physiol. 2008; 294: L110 ‐ L120.
dc.identifier.citedreferenceFranzdottir SR, Axelsson IT, Arason AJ, et al. Airway branching morphogenesis in three dimensional culture. Respir Res. 2010; 11: 162.
dc.identifier.citedreferenceDye BR, Dedhia PH, Miller AJ, et al. A bioengineered niche promotes in vivo engraftment and maturation of pluripotent stem cell derived human lung organoids. Elife. 2016; 5: e19732.
dc.identifier.citedreferenceChen Y, Feng J, Zhao S, et al. Long‐term engraftment promotes differentiation of alveolar epithelial cells from human embryonic stem cell derived lung organoids. Stem Cells Dev. 2018; 27: 1339 ‐ 1349.
dc.identifier.citedreferenceAcosta JM, Thebaud B, Castillo C, et al. Novel mechanisms in murine nitrofen‐induced pulmonary hypoplasia: FGF‐10 rescue in culture. Am J Physiol Lung Cell Mol Physiol. 2001; 281: L250 ‐ L257.
dc.identifier.citedreferenceTan Q, Choi KM, Sicard D, Tschumperlin DJ. Human airway organoid engineering as a step toward lung regeneration and disease modeling. Biomaterials. 2017; 113: 118 ‐ 132.
dc.identifier.citedreferenceJesudason EC, Connell MG, Fernig DG, Lloyd DA, Losty PD. In vitro effects of growth factors on lung hypoplasia in a model of congenital diaphragmatic hernia. J Pediatr Surg. 2000; 35: 914 ‐ 922.
dc.identifier.citedreferencePutnam LR, Harting MT, Tsao K, et al. Congenital diaphragmatic hernia defect size and infant morbidity at discharge. Pediatrics. 2016; 138: e20162043.
dc.identifier.citedreferenceCameron DB, Graham DA, Milliren CE, et al. Quantifying the burden of interhospital cost variation in pediatric surgery: implications for the prioritization of comparative effectiveness research. JAMA Pediatr. 2017; 171: e163926.
dc.identifier.citedreferenceKays DW, Islam S, Larson SD, Perkins J, Talbert JL. Long‐term maturation of congenital diaphragmatic hernia treatment results toward development of a severity‐specific treatment algorithm. Ann Surg. 2013; 258: 638 ‐ 645.
dc.identifier.citedreferenceHarrison MR, Keller RL, Hawgood SB, et al. A randomized trial of fetal endoscopic tracheal occlusion for severe fetal congenital diaphragmatic hernia. N Engl J Med. 2003; 349: 1916 ‐ 1924.
dc.identifier.citedreferenceKunisaki SM, Barnewolt CE, Estroff JA, et al. Ex utero intrapartum treatment with extracorporeal membrane oxygenation for severe congenital diaphragmatic hernia. J Pediatr Surg. 2007; 42: 98 ‐ 104.
dc.identifier.citedreferenceHarting MT, Hollinger L, Tsao K, et al. Aggressive surgical management of congenital diaphragmatic hernia: worth the effort? A multicenter, prospective, cohort study. Ann Surg. 2018; 267: 977 ‐ 982.
dc.identifier.citedreferenceMuratore CS, Kharasch V, Lund DP, et al. Pulmonary morbidity in 100 survivors of congenital diaphragmatic hernia monitored in a multidisciplinary clinic. J Pediatr Surg. 2001; 36: 133 ‐ 140.
dc.identifier.citedreferenceDao DT, Hayden LP, Buchmiller TL, et al. Longitudinal analysis of pulmonary function in survivors of congenital diaphragmatic hernia. J Pediatr. 2019; 216: 158 ‐ 164.
dc.identifier.citedreferenceRottier R, Tibboel D. Fetal lung and diaphragm development in congenital diaphragmatic hernia. Semin Perinatol. 2005; 29: 86 ‐ 93.
dc.identifier.citedreferenceYu L, Hernan RR, Wynn J, et al. The influence of genetics in congenital diaphragmatic hernia. Semin Perinatol. 2019; 44: 151169.
dc.identifier.citedreferenceWynn J, Yu L, Chung WK. Genetic causes of congenital diaphragmatic hernia. Semin Fetal Neonatal Med. 2014; 19: 324 ‐ 330.
dc.identifier.citedreferenceAmeis D, Khoshgoo N, Keijzer R. Abnormal lung development in congenital diaphragmatic hernia. Semin Pediatr Surg. 2017; 26: 123 ‐ 128.
dc.identifier.citedreferenceRussell MK, Longoni M, Wells J, et al. Congenital diaphragmatic hernia candidate genes derived from embryonic transcriptomes. Proc Natl Acad Sci USA. 2012; 109: 2978 ‐ 2983.
dc.identifier.citedreferenceVeenma DC, de Klein A, Tibboel D. Developmental and genetic aspects of congenital diaphragmatic hernia. Pediatr Pulmonol. 2012; 47: 534 ‐ 545.
dc.identifier.citedreferenceAckerman KG, Herron BJ, Vargas SO, et al. Fog2 is required for normal diaphragm and lung development in mice and humans. PLoS Genet. 2005; 1: 58 ‐ 65.
dc.identifier.citedreferenceYu L, Wynn J, Cheung YH, et al. Variants in GATA4 are a rare cause of familial and sporadic congenital diaphragmatic hernia. Hum Genet. 2013; 132: 285 ‐ 292.
dc.identifier.citedreferenceNelson CM, Gleghorn JP, Pang MF, et al. Microfluidic chest cavities reveal that transmural pressure controls the rate of lung development. Development. 2017; 144: 4328 ‐ 4335.
dc.identifier.citedreferenceWells LJ. A study of closure of the pleuropericardial and pleuroperitoneal canals in the human embryo. Anat Rec. 1947; 97: 428.
dc.identifier.citedreferenceHarrison MR, Jester JA, Ross NA. Correction of congenital diaphragmatic hernia in utero. I. The model: intrathoracic balloon produces fatal pulmonary hypoplasia. Surgery. 1980; 88: 174 ‐ 182.
dc.identifier.citedreferenceLazar DA, Ruano R, Cass DL, et al. Defining "liver‐up": does the volume of liver herniation predict outcome for fetuses with isolated left‐sided congenital diaphragmatic hernia? J Pediatr Surg. 2012; 47: 1058 ‐ 1062.
dc.identifier.citedreferenceJesudason EC. Small lungs and suspect smooth muscle: congenital diaphragmatic hernia and the smooth muscle hypothesis. J Pediatr Surg. 2006; 41: 431 ‐ 435.
dc.identifier.citedreferenceKeijzer R, Liu J, Deimling J, Tibboel D, Post M. Dual‐hit hypothesis explains pulmonary hypoplasia in the nitrofen model of congenital diaphragmatic hernia. Am J Pathol. 2000; 156: 1299 ‐ 1306.
dc.identifier.citedreferenceJesudason EC, Losty PD, Lloyd DA. Pulmonary hypoplasia: alternative pathogenesis and antenatal therapy in diaphragmatic hernia. Arch Dis Child Fetal Neonatal Ed. 2000; 82: F172.
dc.identifier.citedreferenceDerderian SC, Jayme CM, Cheng LS, Keller RL, Moon‐Grady AJ, MacKenzie T. Mass effect alone may not explain pulmonary vascular pathology in severe congenital diaphragmatic hernia. Fetal Diagn Ther. 2016; 39: 117 ‐ 124.
dc.identifier.citedreferenceGuilbert TW, Gebb SA, Shannon JM. Lung hypoplasia in the nitrofen model of congenital diaphragmatic hernia occurs early in development. Am J Physiol Lung Cell Mol Physiol. 2000; 279: L1159 ‐ L1171.
dc.identifier.citedreferenceCorreia‐Pinto J, Baptista MJ, Pedrosa C, Estevão‐Costa J, Flake AW, Leite‐Moreira AF. Fetal heart development in the nitrofen‐induced CDH rat model: the role of mechanical and nonmechanical factors. J Pediatr Surg. 2003; 38: 1444 ‐ 1451.
dc.identifier.citedreferenceJay PY, Bielinska M, Erlich JM, et al. Impaired mesenchymal cell function in Gata4 mutant mice leads to diaphragmatic hernias and primary lung defects. Dev Biol. 2007; 301: 602 ‐ 614.
dc.identifier.citedreferenceJiang G, Di Bernardo J, Maiden MM, et al. Human transgene‐free amniotic‐fluid‐derived induced pluripotent stem cells for autologous cell therapy. Stem Cells Dev. 2014; 23: 2613 ‐ 2625.
dc.identifier.citedreferenceJiang G, Herron TJ, Di Bernardo J, et al. Human cardiomyocytes prior to birth by integration‐free reprogramming of amniotic fluid cells. Stem Cells Translational Medicine. 2016; 5: 1595 ‐ 1606.
dc.identifier.citedreferenceItskovitz‐Eldor J, Schuldiner M, Karsenti D, et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med. 2000; 6: 88 ‐ 95.
dc.identifier.citedreferenceDye BR, Hill DR, Ferguson MA, et al. In vitro generation of human pluripotent stem cell derived lung organoids. Elife. 2015; 4: e05098.
dc.identifier.citedreferenceMiller AJ, Dye BR, Ferrer‐Torres D, et al. Generation of lung organoids from human pluripotent stem cells in vitro. Nat Protoc. 2019; 14: 518 ‐ 540.
dc.identifier.citedreferenceTse JM, Cheng G, Tyrrell JA, et al. Mechanical compression drives cancer cells toward invasive phenotype. Proc Natl Acad Sci USA. 2012; 109: 911 ‐ 916.
dc.identifier.citedreferenceFox ZD, Jiang G, Ho KKY, Walker KA, Liu AP, Kunisaki SM. Fetal lung transcriptome patterns in an ex vivo compression model of diaphragmatic hernia. J Surg Res. 2018; 231: 411 ‐ 420.
dc.identifier.citedreferenceOlver RE, Walters DV, Wilson SM. Developmental regulation of lung liquid transport. Annu Rev Physiol. 2004; 66: 77 ‐ 101.
dc.identifier.citedreferenceHuang DW, Sherman BT, Tan Q, et al. The DAVID gene functional classification tool: a novel biological module‐centric algorithm to functionally analyze large gene lists. Genome Biol. 2007; 8: R183.
dc.identifier.citedreferenceMarconett CN, Zhou B, Sunohara M, et al. Cross‐species transcriptome profiling identifies new alveolar epithelial type I cell‐specific genes. Am J Respir Cell Mol Biol. 2017; 56: 310 ‐ 321.
dc.identifier.citedreferenceKho AT, Bhattacharya S, Tantisira KG, et al. Transcriptomic analysis of human lung development. Am J Respir Crit Care Med. 2010; 181: 54 ‐ 63.
dc.identifier.citedreferenceKool HM, Burgisser PE, Edel GG, et al. Inhibition of retinoic acid signaling induces aberrant pericyte coverage and differentiation resulting in vascular defects in congenital diaphragmatic hernia. Am J Physiol Lung Cell Mol Physiol. 2019; 317: L317 ‐ L331.
dc.identifier.citedreferenceYu L, Wynn J, Ma L, et al. De novo copy number variants are associated with congenital diaphragmatic hernia. J Med Genet. 2012; 49: 650 ‐ 659.
dc.identifier.citedreferenceBargy F, Beaudoin S, Barbet P. Fetal lung growth in congenital diaphragmatic hernia. Fetal Diagn Ther. 2006; 21: 39 ‐ 44.
dc.identifier.citedreferenceKitagawa M, Hislop A, Boyden EA, Reid L. Lung hypoplasia in congenital diaphragmatic hernia. A quantitative study of airway, artery, and alveolar development. Br J Surg. 1971; 58: 342 ‐ 346.
dc.identifier.citedreferenceHeerema AE, Rabban JT, Sydorak RM, Harrison MR, Jones KD. Lung pathology in patients with congenital diaphragmatic hernia treated with fetal surgical intervention, including tracheal occlusion. Pediatr Dev Pathol. 2003; 6: 536 ‐ 546.
dc.identifier.citedreferenceNakao Y, Ueki R. Congenital diaphragmatic hernia induced by nitrofen in mice and rats: characteristics as animal model and pathogenetic relationship between diaphragmatic hernia and lung hypoplasia. Congenit Anom. 1987; 27: 397 ‐ 417.
dc.identifier.citedreferencevan Loenhout RB, Tibboel D, Post M, Keijzer R. Congenital diaphragmatic hernia: comparison of animal models and relevance to the human situation. Neonatology. 2009; 96: 137 ‐ 149.
dc.identifier.citedreferenceWaters CM, Roan E, Navajas D. Mechanobiology in lung epithelial cells: measurements, perturbations, and responses. Compr Physiol. 2012; 2: 1 ‐ 29.
dc.identifier.citedreferenceSanchez‐Esteban J, Wang Y, Cicchiello LA, Rubin LP. Cyclic mechanical stretch inhibits cell proliferation and induces apoptosis in fetal rat lung fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2002; 282: L448 ‐ L456.
dc.identifier.citedreferenceHerriges MJ, Tischfield DJ, Cui Z, et al. The NANCI‐Nkx2.1 gene duplex buffers Nkx2.1 expression to maintain lung development and homeostasis. Genes Dev. 2017; 31: 889 ‐ 903.
dc.identifier.citedreferenceLittle DR, Gerner‐Mauro KN, Flodby P, et al. Transcriptional control of lung alveolar type 1 cell development and maintenance by NK homeobox 2–1. Proc Natl Acad Sci USA. 2019; 116: 20545 ‐ 20555.
dc.identifier.citedreferenceWan H, Dingle S, Xu Y, et al. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J Biol Chem. 2005; 280: 13809 ‐ 13816.
dc.identifier.citedreferenceStone KC, Mercer RR, Gehr P, Stockstill B, Crapo JD. Allometric relationships of cell numbers and size in the mammalian lung. Am J Respir Cell Mol Biol. 1992; 6: 235 ‐ 243.
dc.identifier.citedreferenceNguyen TM, Jimenez J, Rendin LE, et al. The proportion of alveolar type 1 cells decreases in murine hypoplastic congenital diaphragmatic hernia lungs. PLoS One. 2019; 14: e0214793.
dc.identifier.citedreferenceBarkauskas CE, Cronce MJ, Rackley CR, et al. Type 2 alveolar cells are stem cells in adult lung. J Clin Invest. 2013; 123: 3025 ‐ 3036.
dc.identifier.citedreferenceKuhn H, Zobel C, Vollert G, et al. High amplitude stretching of ATII cells and fibroblasts results in profibrotic effects. Exp Lung Res. 2019; 45: 167 ‐ 174.
dc.identifier.citedreferenceKitterman JA. The effects of mechanical forces on fetal lung growth. Clin Perinatol. 1996; 23: 727 ‐ 740.
dc.identifier.citedreferenceNicolini U, Fisk NM, Rodeck CH, Talbert DG, Wigglesworth JS. Low amniotic pressure in oligohydramnios—is this the cause of pulmonary hypoplasia? Am J Obstet Gynecol. 1989; 161: 1098 ‐ 1101.
dc.identifier.citedreferenceVarner VD, Gleghorn JP, Miller E, Radisky DC, Nelson CM. Mechanically patterning the embryonic airway epithelium. Proc Natl Acad Sci USA. 2015; 112: 9230 ‐ 9235.
dc.identifier.citedreferenceInanlou MR, Baguma‐Nibasheka M, Kablar B. The role of fetal breathing‐like movements in lung organogenesis. Histol Histopathol. 2005; 20: 1261 ‐ 1266.
dc.identifier.citedreferenceNobuhara KK, Wilson JM. The effect of mechanical forces on in utero lung growth in congenital diaphragmatic hernia. Clin Perinatol. 1996; 23: 741 ‐ 752.
dc.identifier.citedreferenceKoos BJ, Rajaee A. Fetal breathing movements and changes at birth. Adv Exp Med Biol. 2014; 814: 89 ‐ 101.
dc.identifier.citedreferenceJesudason EC, Smith NP, Connell MG, et al. Developing rat lung has a sided pacemaker region for morphogenesis‐related airway peristalsis. Am J Respir Cell Mol Biol. 2005; 32: 118 ‐ 127.
dc.identifier.citedreferenceSchittny JC, Miserocchi G, Sparrow MP. Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants. Am J Respir Cell Mol Biol. 2000; 23: 11 ‐ 18.
dc.identifier.citedreferenceSeravalli V, Jelin EB, Miller JL, Tekes A, Vricella L, Baschat AA. Fetoscopic tracheal occlusion for treatment of non‐isolated congenital diaphragmatic hernia. Prenat Diagn. 2017; 37: 1046 ‐ 1049.
dc.identifier.citedreferenceChapin CJ, Ertsey R, Yoshizawa J, et al. Congenital diaphragmatic hernia, tracheal occlusion, thyroid transcription factor‐1, and fetal pulmonary epithelial maturation. Am J Physiol Lung Cell Mol Physiol. 2005; 289: L44 ‐ L52.
dc.identifier.citedreferenceUnbekandt M, del Moral PM, Sala FG, Bellusci S, Warburton D, Fleury V. Tracheal occlusion increases the rate of epithelial branching of embryonic mouse lung via the FGF10‐FGFR2b‐Sprouty2 pathway. Mech Dev. 2008; 125: 314 ‐ 324.
dc.identifier.citedreferenceDanzer E, Robinson LE, Davey MG, et al. Tracheal occlusion in fetal rats alters expression of mesenchymal nuclear transcription factors without affecting surfactant protein expression. J Pediatr Surg. 2006; 41: 774 ‐ 780.
dc.identifier.citedreferenceNtokou A, Klein F, Dontireddy D, et al. Characterization of the platelet‐derived growth factor receptor‐alpha‐positive cell lineage during murine late lung development. Am J Physiol Lung Cell Mol Physiol. 2015; 309: L942 ‐ L958.
dc.identifier.citedreferenceEndale M, Ahlfeld S, Bao E, et al. Temporal, spatial, and phenotypical changes of PDGFRalpha expressing fibroblasts during late lung development. Dev Biol. 2017; 425: 161 ‐ 175.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
sct312826.pdf
Size:
9.442MB
Format:
PDF
View/Open
Name:
sct312826_am.pdf
Size:
15.68MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.