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Stem Cell Therapy for Neonatal Lung Diseases

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Regenerative Medicine - from Protocol to Patient

Abstract

Despite advances in perinatal care, neonatal lung diseases characterized by disrupted alveolar and vascular development, such as bronchopulmonary dysplasia and congenital diaphragmatic hernia, remain a therapeutic challenge and economic burden with long-term consequences that may affect a lifetime. Stem cell therapies appear promising for yet untreatable diseases. Several studies have already proven stem cell efficacy in a variety of experimental settings, including neonatal lung diseases. Among stem cells, mesenchymal stem cells and endothelial progenitors cells may offer new hope to the neonatal population. These two cell types share a similar mechanism of action, including recruitment to site of injury and subsequent paracrine secretion of bioactive molecule and microvesicles. The evidence of a paracrine mechanism as the crucial effector of stem cells is directing research towards cell-free products, that may further change the face of regenerative medicine. Current clinical translation of regenerative medicine is mainly involving mesenchymal stem cells, thanks to their unique properties and extensive preclinical evidence. Given the essential role of vasculogenesis in lung development, further insight into endothelial progenitor cells may prove them as an important therapeutic option in neonatal lung diseases. Eventually co-transplantation of mesenchymal stem cells and endothelial progenitors cells may increase their therapeutic potential.

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References

  • Acker SN, Seedorf GJ, Abman SH, Nozik-Grayck E, Partrick DA, Gien J (2013) Pulmonary artery endothelial cell dysfunction and decreased populations of highly proliferative endothelial cells in experimental congenital diaphragmatic hernia. Am J Physiol Lung Cell Mol Physiol 305:L943–L952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Acker SN, Kinsella JP, Abman SH, Gien J (2014) Vasopressin improves hemodynamic status in infants with congenital diaphragmatic hernia. J Pediatr 165:53–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akyurekli C, Le Y, Richardson RB, Fergusson D, Tay J, Allan DS (2015) A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles. Stem Cell Rev 11:150–160

    Article  CAS  PubMed  Google Scholar 

  • Alagesan S, Griffin MD (2014) Autologous and allogeneic mesenchymal stem cells in organ transplantation: what do we know about their safety and efficacy? Curr Opin Organ Transplant 19:65–72

    Article  CAS  PubMed  Google Scholar 

  • Albertine KH (2015) Utility of large-animal models of BPD: chronically ventilated preterm lambs. Am J Physiol Lung Cell Mol Physiol 15(308):L983–L1001

    Article  CAS  Google Scholar 

  • Alphonse RS, Vadivel A, Fung M (2014) Existence, functional impairment, and lung repair potential of endothelial colony-forming cells in oxygen-induced arrested alveolar growth. Circulation 129:2144–2157

    Article  PubMed  PubMed Central  Google Scholar 

  • Alvarez DF, Huang L, King JA, ElZarrad MK, Yoder MC, Stevens T (2008) Lung microvascular endothelium is enriched with progenitor cells that exhibit vasculogenic capacity. Am J Physiol Lung Cell Mol Physiol 294:L419–L430

    Article  CAS  PubMed  Google Scholar 

  • Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967

    Article  CAS  PubMed  Google Scholar 

  • Aslam M, Baveja R, Liang OD (2009) Bone marrow stromal cells attenuate lung injury in a murine model of neonatal chronic lung disease. Am J Respir Crit Care Med 180:1122–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker CD, Ryan SL, Ingram DA, Seedorf GJ, Abman SH, Balasubramaniam V (2009) Endothelial colony-forming cells from preterm infants are increased and more susceptible to hyperoxia. Am J Respir Crit Care Med 180:454–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Baker CD, Balasubramaniam V, Mourani PM, Sontag MK, Black CP, Ryan SL et al (2012) Cord blood angiogenic progenitor cells are decreased in bronchopulmonary dysplasia. Eur Respir J 40:1516–1522

    Article  PubMed  Google Scholar 

  • Baker CD, Seedorf GJ, Wisniewski BL, Black CP, Ryan SL, Balasubramaniam V et al (2013a) Endothelial colony-forming cell conditioned media promote angiogenesis in vitro and prevent pulmonary hypertension in experimental bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 305:L73–L81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker CD, Black CP, Ryan SL, Balasubramaniam V, Abman SH (2013b) Cord blood endothelial colony-forming cells from newborns with congenital diaphragmatic hernia. J Pediatr 163:905–907

    Article  PubMed  PubMed Central  Google Scholar 

  • Baraldi E, Bonetto G, Zacchello F, Filippone M (2005) Low exhaled nitric oxide in school-age children with bronchopulmonary dysplasia and airflow limitation. Am J Respir Crit Care Med 171:68–72

    Article  PubMed  Google Scholar 

  • Batsali AK, Kastrinaki MC, Papadaki HA (2013) Mesenchymal stem cells derived from Wharton’s Jelly of the umbilical cord: Biological properties and emerging clinical applications. Curr Stem Cell Res Ther 8:144–155

    Article  CAS  PubMed  Google Scholar 

  • Beam KS, Aliaga S, Ahlfeld SK, Cohen-Wolkowiez M, Smith PB, Laughon MM (2014) A systematic review of randomized controlled trials for the prevention of bronchopulmonary dysplasia in infants. J Perinatol 34:705–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berger J, Bhandari V (2014) Animal models of bronchopulmonary dysplasia. The term mouse models. Am J Physiol Lung Cell Mol Physiol 307:L936–L947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borghesi A, Massa M, Campanelli R, Bollani L, Tzialla C, Figar TA et al (2009) Circulating endothelial progenitor cells in preterm infants with bronchopulmonary dysplasia. Am J Respir Crit Care Med 180:540–546

    Article  PubMed  Google Scholar 

  • Boström H, Willetts K, Pekny M, Levéen P, Lindahl P, Hedstrand H et al (1996) PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85:863–873

    Article  PubMed  Google Scholar 

  • Beurskens LW, Schrijver LH, Tibboel D, Wildhagen MF, Knapen MF, Lindemans J et al (2013) Dietary vitamin A intake below the recommended daily intake during pregnancy and the risk of congenital diaphragmatic hernia in the offspring. Birth Defects Res A Clin Mol Teratol 97:60–66

    Article  CAS  PubMed  Google Scholar 

  • Beurskens LW, Tibboel D, Lindemans J, Duvekot JJ, Cohen-Overbeek TE, Veenma DC et al (2010) Retinol status of newborn infants is associated with congenital diaphragmatic hernia. Pediatrics 126:712–720

    Article  PubMed  Google Scholar 

  • Bouman NH, Koot HM, Tibboel D, Hazebroek FWJ (2000) Children with congenital diaphragmatic hernia are at risk for lower levels of cognitive functioning and increased emotional and behavioral problems. Eur J Pediatr Surg 10:3e7

    Article  Google Scholar 

  • Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M, Park TS et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313

    Article  CAS  PubMed  Google Scholar 

  • Case J, Mead LE, Bessler WK, Prater D, White HA, Saadatzadeh MR et al (2007) Human CD34+AC133+VEGFR-2+cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35:1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Castro-Malaspina H, Gay RE, Resnick G, Kapoor N, Meyers P et al (1980) Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 56:289–301

    CAS  PubMed  Google Scholar 

  • Chang JC, Summer R, Sun X, Fitzsimmons K, Fine A (2005) Evidence that bone marrow cells do not contribute to the alveolar epithelium. Am J Respir Cell Mol Biol 33:335–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang YS, Oh W, Choi SJ, Sung DK, Kim SY, Choi EY et al (2009) Human umbilical cord blood-derived mesenchymal stem cells attenuate hyperoxia-induced lung injury in neonatal rats. Cell Transplant 18:869–886

    Article  PubMed  Google Scholar 

  • Chang YS, Choi SJ, Sung DK, Kim SY, Oh W, Yang YS et al (2011) Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells dose-dependently attenuates hyperoxia-induced lung injury in neonatal rats. Cell Transplant 20:1843–1854

    Article  PubMed  Google Scholar 

  • Chang YS, Choi SJ, Ahn SY, Sung DK, Sung SI, Yoo HS et al (2013) Timing of umbilical cord blood derived mesenchymal stem cells transplantation determines therapeutic efficacy in the neonatal hyperoxic lung injury. PLoS One 8:e52419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang YS, Ahn SY, Yoo HS, Sung SI, Choi SJ, Oh WI et al. (2014) Mesenchymal stem cells for bronchopulmonary dysplasia: phase 1 dose-escalation clinical trial. J Pediatr 164:966–972.e6.

    Google Scholar 

  • Chaput N, Thery C (2011) Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 33:419–440

    Article  CAS  PubMed  Google Scholar 

  • Chavakis E, Aicher A, Heeschen C, Sasaki K, Kaiser R, El Makhfi N et al (2005) Role of beta2-integrins for homing and neovascularization capacity of endothelial progenitor cells. J Exp Med 201:63–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiu PP (2014) New insights into congenital diaphragmatic hernia – a surgeon’s introduction to CDH animal models. Front Pediatr 2:36

    Article  PubMed  PubMed Central  Google Scholar 

  • Chua F, Gauldie J, Laurent GJ (2005) Pulmonary fibrosis: searching for model answers. Am J Respir Cell Mol Biol 33:9–13

    Article  CAS  PubMed  Google Scholar 

  • Clark J, Alvarez DF, Alexeyev M, King JA, Huang L, Yoder MC et al (2008) Regulatory role for nucleosome assembly protein-1 in the proliferative and vasculogenic phenotype of pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 294:L431–L439

    Article  CAS  PubMed  Google Scholar 

  • Coalson JJ (2003) Pathology of new bronchopulmonary dysplasia. Semin Neonatol 8:73–81

    Article  PubMed  Google Scholar 

  • Cutz E, Chiasson D (2008) Chronic lung disease after premature birth. N Engl J Med 14;358:743–745

    Google Scholar 

  • D’Angio CT, Ryan RM (2014) Animal models of bronchopulmonary dysplasia. The preterm and term rabbit models. Am J Physiol Lung Cell Mol Physiol 307:L959–L969

    Article  PubMed  CAS  Google Scholar 

  • Deprest J, De Coppi P (2012) Antenatal management of isolated congenital diaphragmatic hernia today and tomorrow: ongoing collaborative research and development. J Pediatr Surg 47:282–290

    Google Scholar 

  • Darlow BA, Graham PJ (2011). Vitamin A supplementation to prevent mortality and short- and long-term morbidity in very low birthweight infants. Cochrane Database Syst Rev 5(10), CD000501.

    Google Scholar 

  • da Silva ML, Chagastelles PC, Nardi NB (2006) Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119:2204–2213

    Article  CAS  Google Scholar 

  • Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L et al (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110:2440–2448

    Article  CAS  PubMed  Google Scholar 

  • Dignat-George F, Boulanger CM (2011) The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31:27–33

    Article  CAS  PubMed  Google Scholar 

  • Di Bernardo J, Maiden MM, Hershenson MB, Kunisaki SM (2014) Amniotic fluid derived mesenchymal stromal cells augment fetal lung growth in a nitrofen explant model. J Pediatr Surg 49:859–864

    Article  PubMed  Google Scholar 

  • Dmitrieva RI, Minullina IR, Bilibina AA, Tarasova OV, Anisimov SV, Zaritskey AY (2012) Bone marrow- and subcutaneous adipose tissue-derived mesenchymal stem cells: differences and similarities. Cell Cycle 11:377–383

    Article  CAS  PubMed  Google Scholar 

  • Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8:315–317

    Article  CAS  PubMed  Google Scholar 

  • Doyle LW, Anderson PJ (2009) Long-term outcomes of bronchopulmonary dysplasia. Semin Fetal Neonatal Med 14:391–395

    Article  PubMed  Google Scholar 

  • Doyle LW, Halliday HL, Ehrenkranz RA, Davis PG, Sinclair JC (2014) An update on the impact of postnatal systemic corticosteroids on mortality and cerebral palsy in preterm infants: effect modification by risk of bronchopulmonary dysplasia. J Pediatr 165:1258–1260

    Article  CAS  PubMed  Google Scholar 

  • Ehrenkranz RA, Walsh MC, Vohr BR, Jobe AH, Wright LL, Fanaroff AA et al (2005) Validation of the National Institutes of Health consensus definition of broncho-pulmonary dysplasia. Pediatrics 116:1353–1360

    Article  PubMed  Google Scholar 

  • Frisk V, Jakobson LS, Unger S, Trachsel D, O’Brien K (2011) Long-term neurodevelopmental outcomes of congenital diaphragmatic hernia survivors not treated with extracorporeal membrane oxygenation. J Pediatr Surg 46:1309e18

    Article  Google Scholar 

  • Fujinaga H, Baker CD, Ryan SL, Markham NE, Seedorf GJ, Balasubramaniam V et al (2009) Hyperoxia disrupts vascular endothelial growth factor-nitric oxide signaling and decreases growth of endothelial colony-forming cells from preterm infants. Am J Physiol Lung Cell Mol Physiol 297:L1160–L1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fung ME, Thébaud B (2014) Stem cell-based therapy for neonatal lung disease: it is in the juice. Pediatr Res 75:2–7

    Article  PubMed  Google Scholar 

  • Gebler A, Zabel O, Seliger B (2012) The immunomodulatory capacity of mesenchymal stem cells. Trends Mol Med 18:128–134

    Article  CAS  PubMed  Google Scholar 

  • Gehling UM, Ergun S, Schumacher U, Wagener C, Pantel K, Otte M et al (2000) In vitro differentiation of endothelial cells from CD133- positive progenitor cells. Blood 95:3106–3112

    CAS  PubMed  Google Scholar 

  • George DK, Cooney TP, Chiu BK, Thurlbeck WM (1987) Hypoplasia and immaturity of the terminal lung unit (acinus) in congenital diaphragmatic hernia. Am Rev Respir Dis 136:947–950

    Article  CAS  PubMed  Google Scholar 

  • Gong X, Sun Z, Cui D, Xu X, Zhu H, Wang L et al (2014) Isolation and characterization of lung resident mesenchymal stem cells capable of differentiating into alveolar epithelial type II cells. Cell Biol Int 38:405–411

    Article  CAS  PubMed  Google Scholar 

  • Gregory EC, MacDorman MF, Martin JA (2014) Trends in fetal and perinatal mortality in the United States, 2006–2012. NCHS Data Brief 169:1–8

    PubMed  Google Scholar 

  • Guilbert TW, Gebb SA, Shannon JM (2000) Lung hypoplasia in the nitrofen model of congenital diaphragmatic hernia occurs early in development. Am J Physiol Lung Cell Mol Physiol 279:L1159–L1171

    CAS  PubMed  Google Scholar 

  • Guidry CA, Hranjec T, Rodgers BM, Kane B, McGahren ED (2012) Permissive hypercapnia in the management of congenital diaphragmatic hernia: our institutional experience. J Am Coll Surg 214:640–647

    Article  PubMed  PubMed Central  Google Scholar 

  • Gunsilius E, Petzer AL, Duba HC, Kahler CM, Gastl G (2001) Circulating endothelial cells after transplantation. Lancet 357:1449–1450

    Article  CAS  PubMed  Google Scholar 

  • Hansmann G, Fernandez-Gonzalez A, Aslam M, Vitali SH, Martin T, Mitsialis SA et al (2012) Mesenchymal stem cell-mediated reversal of bronchopulmonary dysplasia and associated pulmonary hypertension. Pulm Circ 2:170–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrington KP, Goldman AP (2005) The role of extracorporeal membrane oxygenation in congenital diaphragmatic hernia. Semin Pediatr Surg 14:72–76

    Article  PubMed  Google Scholar 

  • Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR et al (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kitligand. Cell 109:625–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hennessy EM, Bracewell MA, Wood N, Wolke D, Costeloe K, Gibson A et al (2008) Respiratory health in pre-school and school age children following extremely preterm birth. Arch Dis Child 93:1037–1043

    Article  CAS  PubMed  Google Scholar 

  • Hennrick KT, Keeton AG, Nanua S, Kijek TG, Goldsmith AM, Sajjan US et al (2007) Lung Cells from Neonates Show a Mesenchymal Stem Cell Phenotype. Am J Respir Crit Care Med 175:1158–1164

    Google Scholar 

  • Hagensen MK, Raarup MK, Mortensen MB, Thim T, Nyengaard JR, Falk E et al (2012) Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovasc Res 93:223–231

    Article  CAS  PubMed  Google Scholar 

  • Hill JM, Zalos G, Halcox JP, Schenke WH, Waclawiw MA, Quyyumi AA et al (2003) Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 348:593–600

    Article  PubMed  Google Scholar 

  • Hoffman AM, Paxson JA, Mazan MR, Davis AM, Tyagi S, Murthy S et al (2011) Lung-derived mesenchymal stromal cell post-transplantation survival, persistence, paracrine expression, and repair of elastase-injured lung. Stem Cells Dev 20:1779–1792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hood JL, Pan H, Lanza GM, Wickline SA (2009) Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN). Paracrine induction of endothelium by tumor exosomes. Lab Invest 89:1317–1328

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh JY, Fu YS, Chang SJ, Tsuang YH, Wang HW (2010) Functional module analysis reveals differential osteogenic and stemness potentials in human mesenchymal stem cells from bone marrow and Wharton’s jelly of umbilical cord. Stem Cells Dev 19:1895–1910

    Article  CAS  PubMed  Google Scholar 

  • Hsieh JY, Wang HW, Chang SJ, Liao KH, Lee IH, Lin WS et al (2013) Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One 8:e72604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang L, Xu YS, Yu W, Li Y, Chu L, Dong J et al (2010a) Effect of Robo1 on retinal pigment epithelium cells and experimental proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci 51:3193–3204

    Article  PubMed  Google Scholar 

  • Hua J, Yu H, Dong W, Yang C, Gao Z, Lei A et al (2009) Characterization of mesenchymal stem cells (MSCs) from human fetal lung: potential differentiation of germ cells. Tissue Cell 41:448–455

    Article  CAS  PubMed  Google Scholar 

  • Huang XP, Sun Z, Miyagi Y, McDonald Kinkaid H, Zhang L, Weisel RD et al (2010b) Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122:2419–2429

    Article  CAS  PubMed  Google Scholar 

  • Ingenito EP, Tsai L, Murthy S, Tyagi S, Mazan M, Hoffman A (2012) Autologous lung-derived mesenchymal stem cell transplantation in experimental emphysema. Cell Transplant 21:175–189

    Article  PubMed  Google Scholar 

  • Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K et al (2004) Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104:2752–2760

    Article  CAS  PubMed  Google Scholar 

  • Ingram DA, Mead LE, Moore DB, Woodard W, Fenoglio A, Yoder MC (2005) Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105:2783–2786

    Article  CAS  PubMed  Google Scholar 

  • in ‘t Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, et al (2003) Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 88:845–852

    Google Scholar 

  • Islam MN, Das SR, Emin MT, Wei M, Sun L, Westphalen K et al (2012) Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury Nat Med 18:759–765

    Google Scholar 

  • Jankov RP, Negus A, Tanswell AK (2001) Antioxidants as therapy in the newborn: some words of caution. Pediatr Res 50:681–687

    Article  CAS  PubMed  Google Scholar 

  • Jani JC, Nicolaides KH, Gratacós E, Valencia CM, Doné E, Martinez JM et al (2009) Severe diaphragmatic hernia treated by fetal endoscopic tracheal occlusion. Ultrasound Obstet Gynecol 34:304–310

    Article  CAS  PubMed  Google Scholar 

  • Jin HJ, Bae YK, Kim M, Kwon SJ, Jeon HB, Choi SJ et al (2013) Comparative analysis of human mesenchymal stem cells from bone marrow, adipose tissue, and umbilical cord blood as sources of cell therapy. Int J Mol Sci 14:17986–18001

    Article  PubMed  PubMed Central  Google Scholar 

  • Jobe AH, Bancalari E (2001) Bronchopulmonary dysplasia. Am J Respir Crit Care Med 163:1723–1729

    Article  CAS  PubMed  Google Scholar 

  • Kamata S, Usui N, Kamiyama M, Tazuke Y, Nose K, Sawai T et al (2005) Long-term follow-up of patients with high-risk congenital diaphragmatic hernia. J Pediatr Surg 40:1833–1838

    Article  PubMed  Google Scholar 

  • Keijzer R, Liu J, Deimling J, Tibboel D, Post M (2000) Dual-hit hypothesis explains pulmonary hypoplasia in the nitrofen modelof congenital diaphragmatic hernia. Am J Pathol 156:1299–1306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kern S, Eichler H, Stoeve J, Klüter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301

    Article  CAS  PubMed  Google Scholar 

  • Kluth D, Kangah R, Reich P, Tenbrinck R, Tibboel D, Lambrecht W (1990) Nitrofen-induced diaphragmatic hernias in rats: an animal model. J Pediatr Surg 25:850–854

    Article  CAS  PubMed  Google Scholar 

  • Kotecha S (2000) Lung growth: implications for the newborn infant. Arch Dis Child Fetal Neonatal Ed 82:F69–F74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kourembanas S (2015) Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy. Annu Rev Physiol 77:13–27

    Article  CAS  PubMed  Google Scholar 

  • Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R et al (2001) Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369–377

    Article  CAS  PubMed  Google Scholar 

  • Lalu MM, McIntyre L, Pugliese C, Fergusson D, Winston BW, Marshall JC et al (2012) Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. Canadian Critical Care Trials Group. PLoS One 7:e47559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lama VN, Smith L, Badri L, Flint A, Andrei AC, Murray S et al (2007) Evidence for tissue-resident mesenchymal stem cells in human adult lung from studies of transplanted allografts. J Clin Invest 117:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landry JS, Chan T, Lands L, Menzies D (2011) Long-term impact of bronchopulmonary dysplasia on pulmonary function. Can Respir J 18:265–270

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringdén O (2003) HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31:890–896

    Article  PubMed  CAS  Google Scholar 

  • Lee JW, Fang X, Krasnodembskaya A, Howard JP, Matthay MA (2011) Concise review: mesenchymal stem cells for acute lung injury: role of paracrine soluble factors. Stem Cells 29:913–919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee C, Mitsialis SA, Aslam M, Vitali SH, Vergadi E, Konstantinou G et al (2012) Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 126:2601–2611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefkowitz W, Rosenberg SH (2008) Bronchopulmonary dysplasia: pathway from disease to long-term outcome. J Perinatol 28:837–840

    Article  CAS  PubMed  Google Scholar 

  • Li C, Li M, Li S, Xing Y, Yang CY, Li A et al (2015) Progenitors of secondary crest myofibroblasts are developmentally committed in early lung mesoderm. Stem Cells 33:999–1012

    Google Scholar 

  • Li X, Bai J, Ji X, Li R, Xuan Y, Wang Y (2014) Comprehensive characterization of four different populations of human mesenchymal stem cells as regards their immune properties, proliferation and differentiation. Int J Mol Med 34:695–704

    PubMed  PubMed Central  Google Scholar 

  • Lin Y, Weisdorf DJ, Solovey A, Hebbel RP (2000) Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105:71–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin RZ, Moreno-Luna R, Muñoz-Hernandez R, Li D, Jaminet SC, Greene AK et al (2013) Human white adipose tissue vasculature contains endothelial colony-forming cells with robust in vivo vasculogenic potential. Angiogenesis 16:735–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin RZ, Moreno-Luna R, Li D, Jaminet SC, Greene AK, Melero-Martin JM (2014) Human endothelial colony-forming cells serve as trophic mediators for mesenchymal stem cell engraftment via paracrine signaling. Proc Natl Acad Sci U S A 15:10137–10142

    Article  CAS  Google Scholar 

  • Luong C, Rey-Perra J, Vadivel A, Gilmour G, Sauve Y, Koonen D et al (2011) Antenatal sildenafil treatment attenuates pulmonary hypertension in experimental congenital diaphragmatic hernia. Circulation 123:2120–2131

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Xie N, Li W, Yuan B, Shi Y, Wang Y (2014) Immunobiology of mesenchymal stem cells. Cell Death Differ 21:216–225

    Article  CAS  PubMed  Google Scholar 

  • MacDorman MF, Kirmeyer SE, Wilson EC (2012) Fetal and perinatal mortality, United States, 2006. Natl Vital Stat Rep 60:1–22

    Google Scholar 

  • McCulley D, Wienhold M, Sun X (2015) The pulmonary mesenchyme directs lung development. Curr Opin Genet Dev 32:98–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller SM, Glowacki J (2001) Age-related decline in the osteogenic potential of human bone marrow cells cultured in three- dimensional collagen sponges. J Cell Biochem 82:583–590

    Article  CAS  PubMed  Google Scholar 

  • Muller L, Hong CS, Stolz DB, Watkins SC, Whiteside TL (2014) Isolation of biologically-active exosomes from human plasma. J Immunol Methods 411:55–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy MB, Moncivais K, Caplan AI (2013) Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp Mol Med 26:204–219

    Google Scholar 

  • Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D et al (2013) Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 26:204–219

    Article  CAS  PubMed  Google Scholar 

  • Northway WH Jr, Rosan RC, Porter DY (1967) Pulmonary disease following respirator therapy of hyaline-membrane disease. Bronchopulmonary dysplasia. N Engl J Med 276:357–368

    Article  PubMed  Google Scholar 

  • O’Reilly MA, Marr SH, Yee M, McGrath-Morrow SA, Lawrence BP (2008) Neonatal hyperoxia enhances the inflammatory response in adult mice infected with influenza A virus. Am J Respir Crit Care Med 177:1103–1110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • O’Reilly M, Thébaud B (2014) Animal models of bronchopulmonary dysplasia. The term rat models. Am J Physiol Lung Cell Mol Physiol 307:L948–L958

    Article  PubMed  CAS  Google Scholar 

  • O’Toole SJ, Irish MS, Holm BA, Glick PL (1996) Pulmonary vascular abnormalities in congenital diaphragmatic hernia. Clin Perinatol 23:781–794

    PubMed  Google Scholar 

  • Pederiva F, Ghionzoli M, Pierro A, De Coppi P, Tovar JA (2013) Amniotic fluid stem cells rescue both in vitro and in vivo growth, innervation, and motility in nitrofen-exposed hypoplastic rat lungs through paracrine effects. Cell Transplant 22:1683–1694

    Article  CAS  PubMed  Google Scholar 

  • Pierro M, Ionescu L, Montemurro T, Vadivel A, Weissmann G, Oudit G et al (2013) Short-term, long-term and paracrine effect of human umbilical cord-derived stem cells in lung injury prevention and repair in experimental bronchopulmonary dysplasia. Thorax 68:475–484

    Article  PubMed  Google Scholar 

  • Pierro M, Thébaud B (2014) Understanding and treating pulmonary hypertension in congenital diaphragmatic hernia. Semin Fetal Neonatal Med 19:357–363

    Article  CAS  PubMed  Google Scholar 

  • Pober BR (2008) Genetic aspects of human congenital diaphragmatic hernia. Clin Genet 74:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popova AP, Bozyk PD, Goldsmith AM, Linn MJ, Lei J, Bentley JK et al (2010a) Autocrine production of TGF-beta1 promotes myofibroblastic differentiation of neonatal lung mesenchymal stem cells. Am J Physiol Lung Cell Mol Physiol 298:L735–L743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popova AP, Bozyk PD, Bentley JK, Linn MJ, Goldsmith AM, Schumacher RE et al (2010b) Isolation of tracheal aspirate mesenchymal stromal cells predicts bronchopulmonary dysplasia. Pediatrics 126:e1127–e1133

    Article  PubMed  Google Scholar 

  • Popova AP, Bentley JK, Cui TX, Richardson MN, Linn MJ, Lei J et al (2014) Reduced platelet-derived growth factor receptor expression is a primary feature of human bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 307:L231–L239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ralser E, Mueller W, Haberland C, Fink FM, Gutenberger KH, Strobl R et al (2012) Rehospitalization in the first 2 years of life in children born preterm. Acta Paediatr 101:e1–e5

    Article  PubMed  Google Scholar 

  • Ren G, Chen X, Dong F, Li W, Ren X, Zhang Y et al (2012) Concise review: Mesenchymal stem cells and translational medicine: emerging issues. Stem Cells Transl Med 1:51–58

    Article  CAS  PubMed  Google Scholar 

  • Report of Workshop on Bronchopulmonary Dysplasia (1979) NIH publication no. 80–1660. Washington, DC: National Institutes of Health

    Google Scholar 

  • Richardson MR, Yoder MC (2010) Endothelial progenitor cells: quo vadis? J Mol Cell Cardiol 50:266–272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rocha G, Azevedo I, Pinto JC, Guimar ~ aes H (2012) Follow-up of the survivors of congenital diaphragmatic hernia. Early Hum Dev 88:255e8

    Google Scholar 

  • Rombouts WJC, Ploemacher RE (2003) Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 17:160–170

    Article  CAS  PubMed  Google Scholar 

  • Rossor T, Greenough A (2015) Advances in paediatric pulmonary vascular disease associated with bronchopulmonary dysplasia. Expert Rev Respir Med 9:35–43

    Article  CAS  PubMed  Google Scholar 

  • Saugstad OD (2003) Bronchopulmonary dysplasia-oxidative stress and antioxidants. Semin Neonatol 8:39–49

    Article  PubMed  Google Scholar 

  • Sethe S, Scutt A, Stolzing A (2006) Aging of mesenchymal stem cells. Ageing Res Rev 5:91–116

    Article  CAS  PubMed  Google Scholar 

  • Shennan AT1, Dunn MS, Ohlsson A, Lennox K, Hoskins EM (1988) Abnormal pulmonary outcomes in premature infants: prediction from oxygen requirement in the neonatal period. Pediatrics. 82:527–532

    Google Scholar 

  • Schmeisser A, Garlichs CD, Zhang H, Eskafi S, Graffy C, Ludwig J et al (2001) Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in matrigel under angiogenic conditions. Cardiovasc Res 49:671–680

    Article  CAS  PubMed  Google Scholar 

  • Schmidt B, Roberts RS, Davis P, Doyle LW, Barrington KJ, Ohlsson A et al (2006) Caffeine therapy for apnea of prematurity. N Engl J Med 354:2112–2121

    Article  CAS  PubMed  Google Scholar 

  • Shinkai T, Shima H, Solari V, Puri P (2005) Expression of vasoactive mediators during mechanical ventilation in nitrofen induced diaphragmatic hernia in rats. Pediatr Surg Int 21:143–147

    Article  PubMed  Google Scholar 

  • Sluiter I, van der Horst I, van der Voorn P, Boerema-de Munck A, Buscop-van Kempen M, de Krijger R et al (2013) Premature differentiation of vascular smooth muscle cells in human congenital diaphragmatic hernia. Exp Mol Pathol 94:195–202

    Article  CAS  PubMed  Google Scholar 

  • Solodushko V, Fouty B (2007) Proproliferative phenotype of pulmonary microvascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 292:L671–L677

    Article  CAS  PubMed  Google Scholar 

  • Speer CP (2006) Role of inflammation in the evolution of bronchopulmonary dysplasia. J Perinatol 26:S57–S62

    Google Scholar 

  • Spoel M, van der Cammen-van Zijp MH, Hop WC, Tibboel D, de Jongste JC, Ijsselstijn H (2013) Lung function in young adults with congenital diaphragmatic hernia; a longitudinal evaluation. Pediatr Pulmonol 48:130–137

    Article  PubMed  Google Scholar 

  • Stoll BJ, Hansen NI, Bell EF, Shankaran S, Laptook AR, Walsh MC et al (2010) Neonatal outcomes of extremely preterm infants from the NICHD neonatal research network. Pediatrics 126:443–456

    Article  PubMed  PubMed Central  Google Scholar 

  • Sueblinvong V, Loi R, Eisenhauer PL, Bernstein IM, Suratt BT, Spees JL et al (2008) Derivation of lung epithelium from human cord blood-derived mesenchymal stem cells. Am J Respir Crit Care Med 177:701–711

    Article  CAS  PubMed  Google Scholar 

  • Summer R, Fitzsimmons K, Dwyer D, Murphy J, Fine A (2007) Isolation of an adult mouse lung mesenchymal progenitor cell population. Am J Respir Cell Mol Biol 37:152–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutsko RP, Young KC, Ribeiro A, Torres E, Rodriguez M, Hehre D et al (2013) Long-term reparative effects of mesenchymal stem cell therapy following neonatal hyperoxia-induced lung injury. Pediatr Res 73:46–53

    Article  CAS  PubMed  Google Scholar 

  • Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M et al (1999) Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5:434–438

    Article  CAS  PubMed  Google Scholar 

  • Tenbrinck R, Tibboel D, Gaillard JL, Kluth D, Bos AP, Lachmann B, Molenaar JC (1990) Experimentally induced congenital diaphragmatic hernia in rats. J Pediatr Surg 25:426–429

    Article  CAS  PubMed  Google Scholar 

  • Thébaud B, Tibboel D, Rambaud C, Mercier JC, Bourbon JR, Dinh-Xuan AT et al (1999) Vitamin A decreases the incidence and severity of nitrofen-induced congenital diaphragmatic hernia in rats. Am J Physiol 277:L423–L429

    PubMed  Google Scholar 

  • Thirumala S, Goebel WS, Woods EJ (2013) Manufacturing and banking of mesenchymal stem cells. Expert Opin Biol Ther 13:673–691

    Article  CAS  PubMed  Google Scholar 

  • Thompson A, Bhandari V (2008) Pulmonary biomarkers of bronchopulmonary dysplasia. Biomark Insights 3:361–373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Toti P, Buonocore G, Tanganelli P, Catella AM, Palmeri ML, Vatti R et al (1997) Bronchopulmonary dysplasia of the premature baby: an immunohistochemical study. Pediatr Pulmonol 24:22–28

    Article  CAS  PubMed  Google Scholar 

  • Tourneux P, Markham N, Seedorf G, Balasubramaniam V, Abman SH (2009) Inhaled nitric oxide improves lung structure and pulmonary hypertension in a model of bleomycin-induced bronchopulmonary dysplasia in neonatal rats. Am J Physiol Lung Cell Mol Physiol 297:L1103–L1111

    Article  CAS  PubMed  Google Scholar 

  • Tropea KA, Leder E, Aslam M, Lau AN, Raiser DM, Lee JH et al (2012) Bronchoalveolar stem cells increase after mesenchymal stromal cell treatment in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 302:L829–L837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner CG, Klein JD, Steigman SA, Armant M, Nicksa GA, Zurakowski D et al (2011) Preclinical regulatory validation of an engineered diaphragmatic tendon made with amniotic mesenchymal stem cells. J Pediatr Surg 46:57–61

    Article  PubMed  Google Scholar 

  • Urbich C, Heeschen C, Aicher A, Dernbach E, Zeiher AM, Dimmeler S (2003) Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108:2511–2516

    Article  PubMed  Google Scholar 

  • van Balkom BW, de Jong OG, Smits M, Brummelman J, den Ouden K, de Bree PM, et al (2013) Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 2013;9;121:3997–4006, S1–15

    Google Scholar 

  • van Haaften T, Byrne R, Bonnet S et al (2009) Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Crit Care Med 180:1131–1142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Loenhout RB, Tseu I, Fox EK, Huang Z, Tibboel D, Post M, Keijzer R (2012) The pulmonary mesenchymal tissue layer is defective in an in vitro recombinant model of nitrofen-induced lung hypoplasia. Am J Pathol 180:48–60

    Article  PubMed  CAS  Google Scholar 

  • Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H et al (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89:E1–E7

    Article  CAS  PubMed  Google Scholar 

  • Veenma DC, de Klein A, Tibboel D (2012) Developmental and genetic aspects of congenital diaphragmatic hernia. Pediatr Pulmonol 47:534–545

    Article  CAS  PubMed  Google Scholar 

  • Vermont Oxford Network. 2012. VON days pulse oximetry audit summary. Available at: http://www.vtoxford.org/quality/vondays/PO/POResultsSummary.pdf.

  • Walsh MC, Wilson-Costello D, Zadell A, Newman N, Fanaroff A (2003) Safety, reliability, and validity of a physiologic definition of bronchopulmonary dysplasia. J Perinatol 23:451–456

    Article  PubMed  Google Scholar 

  • Walsh MC, Szefler S, Davis J, Allen M, Van Marter L, Abman S et al (2006) Summary proceedings from the bronchopulmonary dysplasia group. Pediatrics 117:S52–S56

    PubMed  Google Scholar 

  • Wang L, Wang XD, Xie GH, Wang L, Hill CK, DeLeve LD (2012) Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats. J Clin Invest 122:1567–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waszak P, Alphonse R, Vadivel A, Ionescu L, Eaton F, Thebaud B (2012) Preconditioning enhances the paracrine effect of mesenchymal stem cells in preventing oxygen-induced neonatal lung injury in rats. Stem Cells Dev 21:2789–2797

    Article  CAS  PubMed  Google Scholar 

  • Watterberg K (2012) Evidence based therapy – postnatal steroids. Clin Perinatol 39:47–59

    Article  PubMed  Google Scholar 

  • Wegmeyer H, Bröske AM, Leddin M, Kuentzer K, Nisslbeck AK, Hupfeld J et al (2013) Mesenchymal stromal cell characteristics vary depending on their origin. Stem Cells Dev 22:2606–2618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wert SE (2011) The Lung. In: Polin RA and Abman SA (ed) Fetal and neonatal physiology, 4th edn. Saunders, Philadelphia, pp 864–875

    Google Scholar 

  • Wright JC, Budd JL, Field DJ, Draper ES (2011) Epidemiology and outcome of congenital diaphragmatic hernia: a 9-year experience. Paediatr Perinat Epidemiol 25:144–149

    Article  PubMed  Google Scholar 

  • Wynn J, Krishnan U, Aspelund G, Zhang Y, Duong J, Stolar CJ et al (2013) Outcomes of congenital diaphragmatic hernia in the modern era of management. J Pediatr 163:114–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Yannarelli G, Dayan V, Pacienza N, Lee CJ, Medin J, Keating A (2013) Human umbilical cord perivascular cells exhibit enhanced cardiomyocyte reprogramming and cardiac function after experimental acute myocardial infarction. Cell Transplant 22:1651–1666

    Article  PubMed  Google Scholar 

  • Yoder BA, Coalson JJ (2014) Animal models of bronchopulmonary dysplasia. The preterm baboon models. Am J Physiol Lung Cell Mol Physiol 307:L970–L977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoder MC, Mead LE, Prater D, Krier TR, Mroueh KN, Li F et al (2007) Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109:1801–1809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuniartha R, Alatas FS, Nagata K, Kuda M, Yanagi Y, Esumi G et al (2014) Therapeutic potential of mesenchymal stem cell transplantation in a nitrofen-induced congenital diaphragmatic hernia rat model. Pediatr Surg Int 30:907–914

    Article  PubMed  Google Scholar 

  • Zhang SJ, Zhang H, Wei YJ, SuWJ LZK, Hou M et al (2006) Adult endothelial progenitor cells from human peripheral blood maintain monocyte/macrophage function throughout in vitro culture. Cell Res 16:577–584

    Article  CAS  PubMed  Google Scholar 

  • Zheng GP, Ge MH, Shu Q, Rojas M, Xu J (2013) Mesenchymal stem cells in the treatment of pediatric diseases. World J Pediatr 9:197–211

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wang D, Liang T, Guo Q, Zhang G (2014) Amniotic fluid-derived mesenchymal stem cells: characteristics and therapeutic applications. Arch Gynecol Obstet 290:223–231

    Article  CAS  PubMed  Google Scholar 

  • Zhu YG, Feng XM, Abbott J, Fang XH, Hao Q, Monsel A et al (2014) Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells 32:116–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu SF, Zhong ZN, Fu XF, Peng DX, Lu GH, Li WH et al (2013) Comparison of cell proliferation, apoptosis, cellular morphology and ultrastructure between human umbilical cord and placenta-derived mesenchymal stem cells. Neurosci Lett 541:77–82

    Article  CAS  PubMed  Google Scholar 

  • Zussman ME, Bagby M, Benson DW, Gupta R, Hirsch R (2012) Pulmonary vascular resistance in repaired congenital diaphragmatic hernia vs. age-matched controls. Pediatr Res 71:697–700

    Article  PubMed  Google Scholar 

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Pierro, M., Ciarmoli, E., Thébaud, B. (2016). Stem Cell Therapy for Neonatal Lung Diseases. In: Steinhoff, G. (eds) Regenerative Medicine - from Protocol to Patient. Springer, Cham. https://doi.org/10.1007/978-3-319-28293-0_14

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