Critical role of vascular endothelial growth factor secreted by mesenchymal stem cells in hyperoxic lung injury

American Journal of Respiratory Cell and Molecular Biology

Volumn 51, Issue 3, 2014, Pages 391-399

  Chang, Yun Sil ^a   Ahn, So Yoon ^a   Jeon, Hong Bae ^b   Sung, Dong Kyung ^a   Kim, Eun Sun ^c   Sung, Se In ^a   Yoo, Hye Soo ^a   Choi, Soo Jin ^b   Oh, Won Il ^b   Park, Won Soon ^a  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b MEDIPOST Co Ltd   (South Korea)

^c CHA University   (South Korea)

Author keywords

Cell transplantation; Lung injury; Newborn; Stem cells; Vascular endothelial growth factor

Indexed keywords

CELL TRANSPLANTATION; LUNG INJURY; NEWBORN; STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, NEUTRALIZING; CELL LINE; CELL TRANSPLANTATION; FETAL BLOOD; GENE EXPRESSION REGULATION; GENE SILENCING; HUMANS; HYDROGEN PEROXIDE; HYPEROXIA; INFLAMMATION; LUNG INJURY; MESENCHYMAL STROMAL CELLS; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUCOSA; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84906858408     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0385OC     Document Type: Article

References (42)

1. Bhandari A, Panitch HB. Pulmonary outcomes in bronchopulmonary dysplasia. Semin Perinatol 2006;30:219-226. (Pubitemid 44062680)
2. Bland RD. Neonatal chronic lung disease in the post-surfactant era. Biol Neonate 2005;88:181-191.
3. 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;18:869-886.
4. 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;20:1843-1854.
5. 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:e52419.
6. 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;54:416-424.
7. Mourani PM, Abman SH. Pulmonary vascular disease in bronchopulmonary dysplasia: pulmonary hypertension and beyond. Curr Opin Pediatr 2013;25:329-337.
8. Thébaud B. Angiogenesis in lung development, injury and repair: implications for chronic lung disease of prematurity. Neonatology 2007;91:291-297.
9. Thébaud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, Hashimoto K, Harry G, Haromy A, Korbutt G, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia-induced lung injury: evidence that angiogenesis participates in alveolarization. Circulation 2005;112:2477-2486.
10. Lassus P, Ristimäki A, Ylikorkala O, Viinikka L, Andersson S. Vascular endothelial growth factor in human preterm lung. Am J Respir Crit Care Med 1999;159:1429-1433. (Pubitemid 29227849)
11. Lassus P, Turanlahti M, Heikkilä P, Andersson LC, Nupponen I, Sarnesto A, Andersson S. Pulmonary vascular endothelial growth factor and Flt-1 in fetuses, in acute and chronic lung disease, and in persistent pulmonary hypertension of the newborn. Am J Respir Crit Care Med 2001;164:1981-1987. (Pubitemid 33152339)
12. Bhatt AJ, Pryhuber GS, Huyck H, Watkins RH, Metlay LA, Maniscalco WM. Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and TIE-2 in human infants dying with bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;164:1971-1980. (Pubitemid 33152338)
13. Kunig AM, Balasubramaniam V, Markham NE, Morgan D, Montgomery G, Grover TR, Abman SH. Recombinant human VEGF treatment enhances alveolarization after hyperoxic lung injury in neonatal rats. Am J Physiol Lung Cell Mol Physiol 2005;289:L529-L535. (Pubitemid 41361662)
14. Kunig AM, Balasubramaniam V, Markham NE, Seedorf G, Gien J, Abman SH. Recombinant human VEGF treatment transiently increases lung edema but enhances lung structure after neonatal hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006;291:L1068-L1078. (Pubitemid 44772069)
15. 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;6:476-486. (Pubitemid 39433582)
16. 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;164:966-972.
17. 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:H2308-H2314.
18. Tögel 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;13:2109-2114.
19. Horie N, Pereira MP, Niizuma K, Sun G, Keren-Gill H, Encarnacion A, Shamloo M, Hamilton SA, Jiang K, Huhn S, et al. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells 2011;29:274-285.
20. Song SY, Chung HM, Sung JH. The pivotal role of VEGF in adipose-derived-stem-cell-mediated regeneration. Expert Opin Biol Ther 2010;10:1529-1537.
21. Lee HJ, Kim KS, Park IH, Kim SU. Human neural stem cells overexpressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS ONE 2007;2:e156.
22. 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;390:834-838.
23. Pierro M, Ionescu L, Montemurro T, Vadivel A, Weissmann G, Oudit G, Emery D, Bodiga S, Eaton F, Péault B, et al. 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 2013;68:475-484.
24. Burst VR, Gillis M, Pütsch F, Herzog R, Fischer JH, Heid P, Müller-Ehmsen J, Schenk K, Fries JW, Baldamus CA, et al. Poor cell survival limits the beneficial impact of mesenchymal stem cell transplantation on acute kidney injury. Nephron, Exp Nephrol 2010;114:e107-e116.
25. Avivi A, Resnick MB, Nevo E, Joel A, Levy AP. Adaptive hypoxic tolerance in the subterranean mole rat Spalax ehrenbergi: the role of vascular endothelial growth factor. FEBS Lett 1999;452:133-140. (Pubitemid 29301732)
26. Maniscalco WM, Watkins RH, D'Angio CT, Ryan RM. Hyperoxic injury decreases alveolar epithelial cell expression of vascular endothelial growth factor (VEGF) in neonatal rabbit lung. Am J Respir Cell Mol Biol 1997;16:557-567. (Pubitemid 127498288)
27. Voelkel NF, Cool C, Taraceviene-Stewart L, Geraci MW, Yeager M, Bull T, Kasper M, Tuder RM. Janus face of vascular endothelial growth factor: the obligatory survival factor for lung vascular endothelium controls precapillary artery remodeling in severe pulmonary hypertension. Crit Care Med 2002;30(5 Suppl):S251-S256. (Pubitemid 34507999)
28. von Degenfeld G, Banfi A, Springer ML, Wagner RA, Jacobi J, Ozawa CR, Merchant MJ, Cooke JP, Blau HM. Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia. FASEB J 2006;20:2657-2659.
29. Cho HJ, Lee N, Lee JY, Choi YJ, Ii M, Wecker A, Jeong JO, Curry C, Qin G, Yoon YS. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med 2007;204:3257-3269.
30. Esquibies AE, Bazzy-Asaad A, Ghassemi F, Nishio H, Karihaloo A, Cantley LG. VEGF attenuates hyperoxic injury through decreased apoptosis in explanted rat embryonic lung. Pediatr Res 2008;63:20-25.
31. Farkas L, Farkas D, Ask K, Möller A, Gauldie J, Margetts P, Inman M, Kolb M. VEGF ameliorates pulmonary hypertension through inhibition of endothelial apoptosis in experimental lung fibrosis in rats. J Clin Invest 2009;119:1298-1311.
32. Marti HH. Vascular endothelial growth factor. Adv Exp Med Biol 2002;513:375-394. (Pubitemid 36332415)
33. Harrigan MR, Ennis SR, Sullivan SE, Keep RF. Effects of intraventricular infusion of vascular endothelial growth factor on cerebral blood flow, edema, and infarct volume. Acta Neurochir (Wien) 2003;145:49-53. (Pubitemid 36174080)
34. Rosenstein JM, Krum JM. New roles for VEGF in nervous tissue: beyond blood vessels. Exp Neurol 2004;187:246-253. (Pubitemid 38610271)
35. 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;44:497-504.
36. Hao Q, Wang L, Tang H. Vascular endothelial growth factor induces protein kinase D-dependent production of proinflammatory cytokines in endothelial cells. Am J Physiol Cell Physiol 2009;296:C821-C827.
37. Manoonkitiwongsa PS, Schultz RL, Whitter EF, Lyden PD. Contraindications of VEGF-based therapeutic angiogenesis: effects on macrophage density and histology of normal and ischemic brains. Vascul Pharmacol 2006;44:316-325.
38. Kim ES, Chang YS, Choi SJ, Kim JK, Yoo HS, Ahn SY, Sung DK, Kim SY, Park YR, Park WS. Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells attenuates Escherichia coli-induced acute lung injury in mice. Respir Res 2011;12:108.
39. Mei SH, McCarter SD, Deng Y, Parker CH, Liles WC, Stewart DJ. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med 2007;4:e269.
40. Gillis P, Savla U, Volpert OV, Jimenez B, Waters CM, Panos RJ, Bouck NP. Keratinocyte growth factor induces angiogenesis and protects endothelial barrier function. J Cell Sci 1999;112:2049-2057. (Pubitemid 29338829)
41. 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;14:17986-18001.
42. Ohki Y, Mayuzumi H, Tokuyama K, Yoshizawa Y, Arakawa H, Mochizuki H, Morikawa A. Hepatocyte growth factor treatment improves alveolarization in a newborn murine model of bronchopulmonary dysplasia. Neonatology 2009;95:332-338.