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Stem Cells for the Prevention of Bronchopulmonary Dysplasia

  • Won Soon ParkEmail author
Chapter
Part of the Respiratory Medicine book series (RM)

Abstract

Bronchopulmonary dysplasia (BPD), a chronic lung disease that occurs in very premature infants, is a major cause of mortality and long-term morbidities in premature infants. Several studies have indicated that stem cell therapy is a promising novel therapeutic modality in preventing and/or treating BPD. This review summarizes recent advances in stem cell research for treating BPD, with a particular focus on preclinical data, covering important issues for clinical translation such as optimal cell type, route, dose, and timing of stem cell therapy and summarizing the results of successful phase I clinical trials of stem cell therapies for BPD.

Keywords

Bronchopulmonary dysplasia Mesenchymal stem cells Cell transplantation Infant Premature 

References

  1. 1.
    Bhandari A, Panitch HB. Pulmonary outcomes in bronchopulmonary dysplasia. Semin Perinatol. 2006;30(4):219–26. doi: 10.1053/j.semperi.2006.05.009. S0146-0005(06)00074-7 [pii].CrossRefPubMedGoogle Scholar
  2. 2.
    Narang I, Rosenthal M, Cremonesini D, Silverman M, Bush A. Longitudinal evaluation of airway function 21 years after preterm birth. Am J Respir Crit Care Med. 2008;178(1):74–80. doi: 10.1164/rccm.200705-701OC.CrossRefPubMedGoogle Scholar
  3. 3.
    Avery ME, Tooley WH, Keller JB, Hurd SS, Bryan MH, Cotton RB, Epstein MF, Fitzhardinge PM, Hansen CB, Hansen TN, et al. Is chronic lung disease in low birth weight infants preventable? A survey of eight centers. Pediatrics. 1987;79(1):26–30.PubMedGoogle Scholar
  4. 4.
    Bregman J, Farrell EE. Neurodevelopmental outcome in infants with bronchopulmonary dysplasia. Clin Perinatol. 1992;19(3):673–94.PubMedGoogle Scholar
  5. 5.
    Walsh MC, Szefler S, Davis J, Allen M, Van Marter L, Abman S, Blackmon L, Jobe A. Summary proceedings from the bronchopulmonary dysplasia group. Pediatrics. 2006;117(3 Pt 2):S52–6. doi: 10.1542/peds.2005-0620I.PubMedGoogle Scholar
  6. 6.
    Chang YS, Oh W, Choi SJ, Sung DK, Kim SY, Choi EY, Kang S, Jin HJ, Yang YS, Park WS. Human umbilical cord blood-derived mesenchymal stem cells attenuate hyperoxia-induced lung injury in neonatal rats. Cell Transplant. 2009;18(8):869–86. doi: 10.3727/096368909X471189. CT-1859 [pii].CrossRefPubMedGoogle Scholar
  7. 7.
    Chang YS, Choi SJ, Sung DK, Kim SY, Oh W, Yang YS, Park WS. Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells dose-dependently attenuates hyperoxia-induced lung injury in neonatal rats. Cell Transplant. 2011;20(11–12):1843–54. doi: 10.3727/096368911X565038.PubMedGoogle Scholar
  8. 8.
    Chang YS, Choi SJ, Ahn SY, Sung DK, Sung SI, Yoo HS, Oh WI, Park WS. Timing of umbilical cord blood derived mesenchymal stem cells transplantation determines therapeutic efficacy in the neonatal hyperoxic lung injury. PLoS One. 2013;8(1):e52419. doi: 10.1371/journal.pone.0052419.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ahn SY, Chang YS, Kim SY, Sung DK, Kim ES, Rime SY, Yu WJ, Choi SJ, Oh WI, Park WS. Long-term (postnatal day 70) outcome and safety of intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells in neonatal hyperoxic lung injury. Yonsei Med J. 2013;54(2):416–24. doi: 10.3349/ymj.2013.54.2.416.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Chang YS, Ahn SY, Jeon HB, Sung DK, Kim ES, Sung SI, Yoo HS, Choi SJ, Oh WI, Park WS. 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):391–9. doi: 10.1165/rcmb.2013-0385OC.CrossRefPubMedGoogle Scholar
  11. 11.
    Ahn SY, Chang YS, Sung DK, Yoo HS, Sung SI, Choi SJ, Park WS. Cell type-dependent variation in paracrine potency determines therapeutic efficacy against neonatal hyperoxic lung injury. Cytotherapy. 2015;17(8):1025–35. doi: 10.1016/j.jcyt.2015.03.008.CrossRefPubMedGoogle Scholar
  12. 12.
    Pierro M, Ionescu L, Montemurro T, Vadivel A, Weissmann G, Oudit G, Emery D, Bodiga S, Eaton F, Peault B, Mosca F, Lazzari L, Thebaud B (2012) 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. doi: 10.1136/thoraxjnl-2012-202323 Google Scholar
  13. 13.
    Aslam M, Baveja R, Liang OD, Fernandez-Gonzalez A, Lee C, Mitsialis SA, Kourembanas S. Bone marrow stromal cells attenuate lung injury in a murine model of neonatal chronic lung disease. Am J Respir Crit Care Med. 2009;180(11):1122–30. doi: 10.1164/rccm.200902-0242OC. 200902-0242OC [pii].CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    van Haaften T, Byrne R, Bonnet S, Rochefort GY, Akabutu J, Bouchentouf M, Rey-Parra GJ, Galipeau J, Haromy A, Eaton F, Chen M, Hashimoto K, Abley D, Korbutt G, Archer SL, Thebaud B. Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Crit Care Med. 2009;180(11):1131–42. doi: 10.1164/rccm.200902-0179OC.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Chang YS, Ahn SY, Yoo HS, Sung SI, Choi SJ, Oh WI, Park WS. Mesenchymal stem cells for bronchopulmonary dysplasia: phase 1 dose-escalation clinical trial. J Pediatr. 2014;164(5):966–72. doi: 10.1016/j.jpeds.2013.12.011. e966.CrossRefPubMedGoogle Scholar
  16. 16.
    Coalson JJ. Pathology of bronchopulmonary dysplasia. Semin Perinatol. 2006;30(4):179–84. doi: 10.1053/j.semperi.2006.05.004.CrossRefPubMedGoogle Scholar
  17. 17.
    Warner BB, Stuart LA, Papes RA, Wispe JR. Functional and pathological effects of prolonged hyperoxia in neonatal mice. Am J Physiol. 1998;275(1 Pt 1):L110–7.PubMedGoogle Scholar
  18. 18.
    deLemos RA, Coalson JJ. The contribution of experimental models to our understanding of the pathogenesis and treatment of bronchopulmonary dysplasia. Clin Perinatol. 1992;19(3):521–39.PubMedGoogle Scholar
  19. 19.
    O'Reilly M, Thebaud B. Animal models of bronchopulmonary dysplasia. The term rat models. Am J Physiol Lung Cell Mol Physiol. 2014;307(12):L948–58. doi: 10.1152/ajplung.00160.2014.CrossRefPubMedGoogle Scholar
  20. 20.
    Alphonse RS, Vadivel A, Fung M, Shelley WC, Critser PJ, Ionescu L, O'Reilly M, Ohls RK, McConaghy S, Eaton F, Zhong S, Yoder M, Thebaud B. Existence, functional impairment, and lung repair potential of endothelial colony-forming cells in oxygen-induced arrested alveolar growth. Circulation. 2014;129(21):2144–57. doi: 10.1161/CIRCULATIONAHA.114.009124.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Waszak P, Alphonse R, Vadivel A, Ionescu L, Eaton F, Thebaud B. Preconditioning enhances the paracrine effect of mesenchymal stem cells in preventing oxygen-induced neonatal lung injury in rats. Stem Cells Dev. 2012;21(15):2789–97. doi: 10.1089/scd.2010.0566.CrossRefPubMedGoogle Scholar
  22. 22.
    Zhang H, Fang J, Su H, Yang M, Lai W, Mai Y, Wu Y. Bone marrow mesenchymal stem cells attenuate lung inflammation of hyperoxic newborn rats. Pediatr Transplant. 2012;16(6):589–98. doi: 10.1111/j.1399-3046.2012.01709.x.CrossRefPubMedGoogle Scholar
  23. 23.
    Zhang H, Fang J, Wu Y, Mai Y, Lai W, Su H. Mesenchymal stem cells protect against neonatal rat hyperoxic lung injury. Expert Opin Biol Ther. 2013;13(6):817–29. doi: 10.1517/14712598.2013.778969.CrossRefPubMedGoogle Scholar
  24. 24.
    Vosdoganes P, Lim R, Koulaeva E, Chan ST, Acharya R, Moss TJ, Wallace EM. Human amnion epithelial cells modulate hyperoxia-induced neonatal lung injury in mice. Cytotherapy. 2013;15(8):1021–9. doi: 10.1016/j.jcyt.2013.03.004.CrossRefPubMedGoogle Scholar
  25. 25.
    Batsali AK, Kastrinaki MC, Papadaki HA, Pontikoglou C. Mesenchymal stem cells derived from Wharton’s Jelly of the umbilical cord: biological properties and emerging clinical applications. Curr Stem Cell Res Ther. 2013;8(2):144–55.CrossRefPubMedGoogle Scholar
  26. 26.
    Hodges RJ, Lim R, Jenkin G, Wallace EM. Amnion epithelial cells as a candidate therapy for acute and chronic lung injury. Stem Cells Int. 2012;2012:709763. doi: 10.1155/2012/709763.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zhang X, Wang H, Shi Y, Peng W, Zhang S, Zhang W, Xu J, Mei Y, Feng Z. Role of bone marrow-derived mesenchymal stem cells in the prevention of hyperoxia-induced lung injury in newborn mice. Cell Biol Int. 2012;36(6):589–94. doi: 10.1042/CBI20110447.CrossRefPubMedGoogle Scholar
  28. 28.
    Fung ME, Thebaud B. Stem cell-based therapy for neonatal lung disease: it is in the juice. Pediatr Res. 2014;75(1–1):2–7. doi: 10.1038/pr.2013.176.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Park HK, Cho KS, Park HY, Shin DH, Kim YK, Jung JS, Park SK, Roh HJ. Adipose-derived stromal cells inhibit allergic airway inflammation in mice. Stem Cells Dev. 2010;19(11):1811–8. doi: 10.1089/scd.2009.0513.CrossRefPubMedGoogle Scholar
  30. 30.
    Balasubramaniam V, Ryan SL, Seedorf GJ, Roth EV, Heumann TR, Yoder MC, Ingram DA, Hogan CJ, Markham NE, Abman SH. Bone marrow-derived angiogenic cells restore lung alveolar and vascular structure after neonatal hyperoxia in infant mice. Am J Physiol Lung Cell Mol Physiol. 2010;298(3):L315–23. doi: 10.1152/ajplung.00089.2009.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Yee M, Vitiello PF, Roper JM, Staversky RJ, Wright TW, McGrath-Morrow SA, Maniscalco WM, Finkelstein JN, O’Reilly MA. Type II epithelial cells are critical target for hyperoxia-mediated impairment of postnatal lung development. Am J Physiol Lung Cell Mol Physiol. 2006;291(5):L1101–11. doi: 10.1152/ajplung.00126.2006.CrossRefPubMedGoogle Scholar
  32. 32.
    Bozyk PD, Popova AP, Bentley JK, Goldsmith AM, Linn MJ, Weiss DJ, Hershenson MB. Mesenchymal stromal cells from neonatal tracheal aspirates demonstrate a pattern of lung-specific gene expression. Stem Cells Dev. 2011;20(11):1995–2007. doi: 10.1089/scd.2010.0494.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Borghesi A, Massa M, Campanelli R, Bollani L, Tzialla C, Figar TA, Ferrari G, Bonetti E, Chiesa G, de Silvestri A, Spinillo A, Rosti V, Stronati M. Circulating endothelial progenitor cells in preterm infants with bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2009;180(6):540–6. doi: 10.1164/rccm.200812-1949OC. 200812-1949OC [pii].CrossRefPubMedGoogle Scholar
  34. 34.
    Baker CD, Balasubramaniam V, Mourani PM, Sontag MK, Black CP, Ryan SL, Abman SH. Cord blood angiogenic progenitor cells are decreased in bronchopulmonary dysplasia. Eur Respir J. 2012;40(6):1516–22. doi: 10.1183/09031936.00017312.CrossRefPubMedGoogle Scholar
  35. 35.
    Tropea KA, Leder E, Aslam M, Lau AN, Raiser DM, Lee JH, Balasubramaniam V, Fredenburgh LE, Alex Mitsialis S, Kourembanas S, Kim CF. Bronchioalveolar stem cells increase after mesenchymal stromal cell treatment in a mouse model of bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2012;302(9):L829–37. doi: 10.1152/ajplung.00347.2011.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Abe S, Lauby G, Boyer C, Rennard SI, Sharp JG. Transplanted BM and BM side population cells contribute progeny to the lung and liver in irradiated mice. Cytotherapy. 2003;5(6):523–33. doi: 10.1080/14653240310003576.CrossRefPubMedGoogle Scholar
  37. 37.
    Berger MJ, Adams SD, Tigges BM, Sprague SL, Wang XJ, Collins DP, McKenna DH. Differentiation of umbilical cord blood-derived multilineage progenitor cells into respiratory epithelial cells. Cytotherapy. 2006;8(5):480–7. doi: 10.1080/14653240600941549.CrossRefPubMedGoogle Scholar
  38. 38.
    Grove JE, Lutzko C, Priller J, Henegariu O, Theise ND, Kohn DB, Krause DS. Marrow-derived cells as vehicles for delivery of gene therapy to pulmonary epithelium. Am J Respir Cell Mol Biol. 2002;27(6):645–51. doi: 10.1165/rcmb.2002-0056RC.CrossRefPubMedGoogle Scholar
  39. 39.
    Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA. 2003;100(14):8407–11. doi: 10.1073/pnas.1432929100. 1432929100 [pii].CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Weiss DJ. Concise review: current status of stem cells and regenerative medicine in lung biology and diseases. Stem Cells. 2014;32(1):16–25. doi: 10.1002/stem.1506.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ahn SY, Chang YS, Park WS. Stem cell therapy for bronchopulmonary dysplasia: bench to bedside translation. J Korean Med Sci. 2015;30(5):509–13. doi: 10.3346/jkms.2015.30.5.509.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Abman SH, Matthay MA. Mesenchymal stem cells for the prevention of bronchopulmonary dysplasia: delivering the secretome. Am J Respir Crit Care Med. 2009;180(11):1039–41. doi: 10.1164/rccm.200909-1330ED.CrossRefPubMedGoogle Scholar
  43. 43.
    Hansmann G, Fernandez-Gonzalez A, Aslam M, Vitali SH, Martin T, Mitsialis SA, Kourembanas S. Mesenchymal stem cell-mediated reversal of bronchopulmonary dysplasia and associated pulmonary hypertension. Pulm Circ. 2012;2(2):170–81. doi: 10.4103/2045-8932.97603.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Lee C, Mitsialis SA, Aslam M, Vitali SH, Vergadi E, Konstantinou G, Sdrimas K, Fernandez-Gonzalez A, Kourembanas S. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation. 2012;126(22):2601–11. doi: 10.1161/CIRCULATIONAHA.112.114173.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Ahn SY, Chang YS, Sung DK, Sung SI, Yoo HS, Lee JH, Oh WI, Park WS. Mesenchymal stem cells prevent hydrocephalus after severe intraventricular hemorrhage. Stroke. 2013;44(2):497–504. doi: 10.1161/STROKEAHA.112.679092.CrossRefPubMedGoogle Scholar
  46. 46.
    Niver D. Bronchopulmonary dysplasia: structural challenges and stem cell treatment potential. Adv Neonatal Care. 2014;14(1):E1–11. doi: 10.1097/ANC.0000000000000050.CrossRefPubMedGoogle Scholar
  47. 47.
    Borok Z, Lubman RL, Danto SI, Zhang XL, Zabski SM, King LS, Lee DM, Agre P, Crandall ED. Keratinocyte growth factor modulates alveolar epithelial cell phenotype in vitro: expression of aquaporin 5. Am J Respir Cell Mol Biol. 1998;18(4):554–61. doi: 10.1165/ajrcmb.18.4.2838.CrossRefPubMedGoogle Scholar
  48. 48.
    Atabai K, Ishigaki M, Geiser T, Ueki I, Matthay MA, Ware LB. Keratinocyte growth factor can enhance alveolar epithelial repair by nonmitogenic mechanisms. Am J Physiol Lung Cell Mol Physiol. 2002;283(1):L163–9. doi: 10.1152/ajplung.00396.2001.CrossRefPubMedGoogle Scholar
  49. 49.
    McCarter SD, Mei SH, Lai PF, Zhang QW, Parker CH, Suen RS, Hood RD, Zhao YD, Deng Y, Han RN, Dumont DJ, Stewart DJ. Cell-based angiopoietin-1 gene therapy for acute lung injury. Am J Respir Crit Care Med. 2007;175(10):1014–26. doi: 10.1164/rccm.200609-1370OC.CrossRefPubMedGoogle Scholar
  50. 50.
    Gupta N, Su X, Popov B, Lee JW, Serikov V, Matthay MA. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol. 2007;179(3):1855–63. 179/3/1855 [pii].CrossRefPubMedGoogle Scholar
  51. 51.
    Folkesson HG, Pittet JF, Nitenberg G, Matthay MA. Transforming growth factor-alpha increases alveolar liquid clearance in anesthetized ventilated rats. Am J Physiol. 1996;271(2 Pt 1):L236–44.PubMedGoogle Scholar
  52. 52.
    Fang X, Neyrinck AP, Matthay MA, Lee JW. Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. J Biol Chem. 2010;285(34):26211–22. doi: 10.1074/jbc.M110.119917.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009;15(1):42–9. doi: 10.1038/nm.1905.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Li J, Huang S, Wu Y, Gu C, Gao D, Feng C, Wu X, Fu X. Paracrine factors from mesenchymal stem cells: a proposed therapeutic tool for acute lung injury and acute respiratory distress syndrome. Int Wound J. 2014;11(2):114–21. doi: 10.1111/iwj.12202.CrossRefPubMedGoogle Scholar
  55. 55.
    Lee JW, Fang X, Krasnodembskaya A, Howard JP, Matthay MA. Concise review: mesenchymal stem cells for acute lung injury: role of paracrine soluble factors. Stem Cells. 2011;29(6):913–9. doi: 10.1002/stem.643.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Deuse T, Peter C, Fedak PW, Doyle T, Reichenspurner H, Zimmermann WH, Eschenhagen T, Stein W, Wu JC, Robbins RC, Schrepfer S. Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction. Circulation. 2009;120(11 Suppl):S247–54. doi: 10.1161/CIRCULATIONAHA.108.843680.CrossRefPubMedGoogle Scholar
  57. 57.
    Khubutiya MS, Vagabov AV, Temnov AA, Sklifas AN. Paracrine mechanisms of proliferative, anti-apoptotic and anti-inflammatory effects of mesenchymal stromal cells in models of acute organ injury. Cytotherapy. 2014;16(5):579–85. doi: 10.1016/j.jcyt.2013.07.017.CrossRefPubMedGoogle Scholar
  58. 58.
    Henning RJ, Sanberg P, Jimenez E. Human cord blood stem cell paracrine factors activate the survival protein kinase Akt and inhibit death protein kinases JNK and p38 in injured cardiomyocytes. Cytotherapy. 2014;16(8):1158–68. doi: 10.1016/j.jcyt.2014.01.415.CrossRefPubMedGoogle Scholar
  59. 59.
    Markel TA, Wang Y, Herrmann JL, Crisostomo PR, Wang M, Novotny NM, Herring CM, Tan J, Lahm T, Meldrum DR. VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Am J Physiol Heart Circ Physiol. 2008;295(6):H2308–14. doi: 10.1152/ajpheart.00565.2008.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Togel F, Zhang P, Hu Z, Westenfelder C. VEGF is a mediator of the renoprotective effects of multipotent marrow stromal cells in acute kidney injury. J Cell Mol Med. 2009;13(8B):2109–14. doi: 10.1111/j.1582-4934.2008.00641.x.CrossRefPubMedGoogle Scholar
  61. 61.
    Horie N, Pereira MP, Niizuma K, Sun G, Keren-Gill H, Encarnacion A, Shamloo M, Hamilton SA, Jiang K, Huhn S, Palmer TD, Bliss TM, Steinberg GK. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells. 2011;29(2):274–85. doi: 10.1002/stem.584.CrossRefPubMedGoogle Scholar
  62. 62.
    Song SY, Chung HM, Sung JH. The pivotal role of VEGF in adipose-derived-stem-cell-mediated regeneration. Expert Opin Biol Ther. 2010;10(11):1529–37. doi: 10.1517/14712598.2010.522987.CrossRefPubMedGoogle Scholar
  63. 63.
    Lehman N, Cutrone R, Raber A, Perry R, Van’t Hof W, Deans R, Ting AE, Woda J. Development of a surrogate angiogenic potency assay for clinical-grade stem cell production. Cytotherapy. 2012;14(8):994–1004. doi: 10.3109/14653249.2012.688945.CrossRefPubMedGoogle Scholar
  64. 64.
    Lee HJ, Kim KS, Park IH, Kim SU. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS One. 2007;2(1), e156. doi: 10.1371/journal.pone.0000156.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Zisa D, Shabbir A, Suzuki G, Lee T. Vascular endothelial growth factor (VEGF) as a key therapeutic trophic factor in bone marrow mesenchymal stem cell-mediated cardiac repair. Biochem Biophys Res Commun. 2009;390(3):834–8. doi: 10.1016/j.bbrc.2009.10.058.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Spencer ND, Gimble JM, Lopez MJ. Mesenchymal stromal cells: past, present, and future. Vet Surg. 2011;40(2):129–39. doi: 10.1111/j.1532-950X.2010.00776.x.CrossRefPubMedGoogle Scholar
  67. 67.
    Sutsko RP, Young KC, Ribeiro A, Torres E, Rodriguez M, Hehre D, Devia C, McNiece I, Suguihara C. Long-term reparative effects of mesenchymal stem cell therapy following neonatal hyperoxia-induced lung injury. Pediatr Res. 2013;73(1):46–53. doi: 10.1038/pr.2012.152.CrossRefPubMedGoogle Scholar
  68. 68.
    Mosna F, Sensebe L, Krampera M. Human bone marrow and adipose tissue mesenchymal stem cells: a user’s guide. Stem Cells Dev. 2010;19(10):1449–70. doi: 10.1089/scd.2010.0140.CrossRefPubMedGoogle Scholar
  69. 69.
    Rocha V, Wagner Jr JE, Sobocinski KA, Klein JP, Zhang MJ, Horowitz MM, Gluckman E. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. Eurocord and international bone marrow transplant registry working committee on alternative donor and stem cell sources. N Engl J Med. 2000;342(25):1846–54. doi: 10.1056/NEJM200006223422501. MJBA-422501 [pii].CrossRefPubMedGoogle Scholar
  70. 70.
    Le Blanc K. Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy. 2003;5(6):485–9. doi: 10.1080/14653240310003611. XLQTCMQP660JW0LU [pii].CrossRefPubMedGoogle Scholar
  71. 71.
    Kern S, Eichler H, Stoeve J, Kluter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006;24(5):1294–301. doi: 10.1634/stemcells.2005-0342.CrossRefPubMedGoogle Scholar
  72. 72.
    Yang SE, Ha CW, Jung M, Jin HJ, Lee M, Song H, Choi S, Oh W, Yang YS. Mesenchymal stem/progenitor cells developed in cultures from UC blood. Cytotherapy. 2004;6(5):476–86. doi: 10.1080/14653240410005041. W4J80FJ7EV8TWW9R [pii].CrossRefPubMedGoogle Scholar
  73. 73.
    Amable PR, Teixeira MV, Carias RB, Granjeiro JM, Borojevic R. Protein synthesis and secretion in human mesenchymal cells derived from bone marrow, adipose tissue and Wharton’s jelly. Stem Cell Res Ther. 2014;5(2):53. doi: 10.1186/scrt442.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med. 2014;12:8. doi: 10.1186/1479-5876-12-8.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Dos-Anjos Vilaboa S, Navarro-Palou M, Llull R. Age influence on stromal vascular fraction cell yield obtained from human lipoaspirates. Cytotherapy. 2014;16(8):1092–7. doi: 10.1016/j.jcyt.2014.02.007.CrossRefPubMedGoogle Scholar
  76. 76.
    Kretlow JD, Jin YQ, Liu W, Zhang WJ, Hong TH, Zhou G, Baggett LS, Mikos AG, Cao Y. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 2008;9:60. doi: 10.1186/1471-2121-9-60.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Jin HJ, Bae YK, Kim M, Kwon SJ, Jeon HB, Choi SJ, Kim SW, Yang YS, Oh W, Chang JW. 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. 2013;14(9):17986–8001. doi: 10.3390/ijms140917986.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Pievani A, Scagliotti V, Russo FM, Azario I, Rambaldi B, Sacchetti B, Marzorati S, Erba E, Giudici G, Riminucci M, Biondi A, Vergani P, Serafini M. Comparative analysis of multilineage properties of mesenchymal stromal cells derived from fetal sources shows an advantage of mesenchymal stromal cells isolated from cord blood in chondrogenic differentiation potential. Cytotherapy. 2014;16(7):893–905. doi: 10.1016/j.jcyt.2014.02.008.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Mayani H, Alvarado-Moreno JA, Flores-Guzman P. Biology of human hematopoietic stem and progenitor cells present in circulation. Arch Med Res. 2003;34(6):476–88. doi: 10.1016/j.arcmed.2003.08.004.CrossRefPubMedGoogle Scholar
  80. 80.
    Kogler G, Critser P, Trapp T, Yoder M. Future of cord blood for non-oncology uses. Bone Marrow Transplant. 2009;44(10):683–97. doi: 10.1038/bmt.2009.287.CrossRefPubMedGoogle Scholar
  81. 81.
    Monz D, Tutdibi E, Mildau C, Shen J, Kasoha M, Laschke MW, Roolfs T, Schmiedl A, Tschernig T, Bieback K, Gortner L. Human umbilical cord blood mononuclear cells in a double-hit model of bronchopulmonary dysplasia in neonatal mice. PLoS One. 2013;8(9):e74740. doi: 10.1371/journal.pone.0074740.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Bieback K, Kinzebach S, Karagianni M. Translating research into clinical scale manufacturing of mesenchymal stromal cells. Stem Cells Int. 2011;2010:193519. doi: 10.4061/2010/193519.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Thebaud B, Abman SH. Bronchopulmonary dysplasia: where have all the vessels gone? Roles of angiogenic growth factors in chronic lung disease. Am J Respir Crit Care Med. 2007;175(10):978–85. doi: 10.1164/rccm.200611-1660PP.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Vosdoganes P, Hodges RJ, Lim R, Westover AJ, Acharya RY, Wallace EM, Moss TJ. Human amnion epithelial cells as a treatment for inflammation-induced fetal lung injury in sheep. Am J obstet Gynecol. 2011;205(2):156.e126–33. doi: 10.1016/j.ajog.2011.03.054.Google Scholar
  85. 85.
    Hodges RJ, Jenkin G, Hooper SB, Allison B, Lim R, Dickinson H, Miller SL, Vosdoganes P, Wallace EM. Human amnion epithelial cells reduce ventilation-induced preterm lung injury in fetal sheep. Am J Obstet Gynecol. 2012;206(5):448.e8–15. doi: 10.1016/j.ajog.2012.02.038.CrossRefGoogle Scholar
  86. 86.
    Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, Brigham KL. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol. 2005;33(2):145–52. doi: 10.1165/rcmb.2004-0330OC. 2004-0330OC [pii].CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Laughon M, Allred EN, Bose C, O’Shea TM, Van Marter LJ, Ehrenkranz RA, Leviton A, Investigators ES. Patterns of respiratory disease during the first 2 postnatal weeks in extremely premature infants. Pediatrics. 2009;123(4):1124–31. doi: 10.1542/peds.2008-0862.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Northway Jr WH, Moss RB, Carlisle KB, Parker BR, Popp RL, Pitlick PT, Eichler I, Lamm RL, Brown Jr BW. Late pulmonary sequelae of bronchopulmonary dysplasia. N Engl J Med. 1990;323(26):1793–9. doi: 10.1056/NEJM199012273232603.CrossRefPubMedGoogle Scholar
  89. 89.
    Landry JS, Chan T, Lands L, Menzies D. Long-term impact of bronchopulmonary dysplasia on pulmonary function. Can Respir J. 2011;18(5):265–70.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Ratner V, Kishkurno SV, Slinko SK, Sosunov SA, Sosunov AA, Polin RA, Ten VS. The contribution of intermittent hypoxemia to late neurological handicap in mice with hyperoxia-induced lung injury. Neonatology. 2007;92(1):50–8. doi: 10.1159/000100086.CrossRefPubMedGoogle Scholar
  91. 91.
    Stoll BJ, Hansen NI, Bell EF, Shankaran S, Laptook AR, Walsh MC, Hale EC, Newman NS, Schibler K, Carlo WA, Kennedy KA, Poindexter BB, Finer NN, Ehrenkranz RA, Duara S, Sanchez PJ, O’Shea TM, Goldberg RN, Van Meurs KP, Faix RG, Phelps DL, Frantz 3rd ID, Watterberg KL, Saha S, Das A, Higgins RD, Eunice Kennedy Shriver National Institute of Child H, Human Development Neonatal Research Network. Neonatal outcomes of extremely preterm infants from the NICHD neonatal research network. Pediatrics. 2010;126(3):443–56. doi: 10.1542/peds.2009-2959.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Anderson PJ, Doyle LW. Neurodevelopmental outcome of bronchopulmonary dysplasia. Semin Perinatol. 2006;30(4):227–32. doi: 10.1053/j.semperi.2006.05.010.CrossRefPubMedGoogle Scholar
  93. 93.
    Dammann O, Leviton A, Bartels DB, Dammann CE. Lung and brain damage in preterm newborns. Are they related? How? Why? Biol Neonate. 2004;85(4):305–13. doi: 10.1159/000078175.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of PediatricsSungkyunkwan University School of Medicine, Samsung Medical CenterKangnam Gu, SeoulSouth Korea

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