Clinical review: Stem cell therapies for acute lung injury/acute respiratory distress syndrome - hope or hype?

Critical Care

Volumn 16, Issue 2, 2012, Pages

  Hayes, Mairead ^a   Curley, Gerard ^a   Ansari, Bilal ^a   Laffey, John G ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CORTICOSTEROID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; LUNG SURFACTANT; NITRIC OXIDE;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; ARTIFICIAL VENTILATION; CELL DIFFERENTIATION; CELL INTERACTION; EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; ENGRAFTMENT; FETAL STEM CELL; HUMAN; IMMUNOMODULATION; MESENCHYMAL STEM CELL; NONHUMAN; PARACRINE SIGNALING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION; THERAPY EFFECT; TREATMENT FAILURE; TREATMENT INDICATION; PATHOPHYSIOLOGY; PROCEDURES; RESPIRATORY DISTRESS SYNDROME, ADULT;

ACUTE LUNG INJURY; HUMANS; RESPIRATORY DISTRESS SYNDROME, ADULT; STEM CELL TRANSPLANTATION;

EID: 84858383411     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/cc10570     Document Type: Review

References (106)

1. Rubenfeld GD, Herridge MS. Epidemiology and outcomes of acute lung injury. Chest 2007, 131:554-562. 10.1378/chest.06-1976, 17296661.
2. Herridge MS, Cheung AM, Tansey CM, Matte-Martyn A, Diaz-Granados N, Al-Saidi F, Cooper AB, Guest CB, Mazer CD, Mehta S, Stewart TE, Barr A, Cook D, Slutsky AS. One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med 2003, 348:683-693. 10.1056/NEJMoa022450, 12594312.
3. England TN. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 2000, 342:1301-1308.
4. Angus DC, Clermont G, Linde-Zwirble WT, Musthafa AA, Dremsizov TT, Lidicker J, Lave JR. Healthcare costs and long-term outcomes after acute respiratory distress syndrome: A phase III trial of inhaled nitric oxide. Crit Care Med 2006, 34:2883-2890.
5. Taylor RW, Zimmerman JL, Dellinger RP, Straube RC, Criner GJ, Davis K, Kelly KM, Smith TC, Small RJ. Low-dose inhaled nitric oxide in patients with acute lung injury: a randomized controlled trial. JAMA 2004, 291:1603-1609. 10.1001/jama.291.13.1603, 15069048.
6. Bernard G, Wheeler A, Naum C, Morris P, Nelson L, Schein R. A placebo controlled, randomised trail of IL-10 in acut lung injury (ALI). Chest 1999, 116(4 Suppl 2):260S.
7. Ortolani O, Conti A, De Gaudio AR, Masoni M, Novelli G. Protective effects of N-acetylcysteine and rutin on the lipid peroxidation of the lung epithelium during the adult respiratory distress syndrome. Shock 2000, 13:14-18. 10.1097/00024382-200013010-00003, 10638663.
8. Domenighetti G, Suter PM, Schaller MD, Ritz R, Perret C. Treatment with N-acetylcysteine during acute respiratory distress syndrome: a randomized, double-blind, placebo-controlled clinical study. J Crit Care 1997, 12:177-182. 10.1016/S0883-9441(97)90029-0, 9459113.
9. Suter PM, Domenighetti G, Schaller MD, Laverriere MC, Ritz R, Perret C. N-acetylcysteine enhances recovery from acute lung injury in man. A randomized, double-blind, placebo-controlled clinical study. Chest 1994, 105:190-194. 10.1378/chest.105.1.190, 8275731.
10. Taut FJ, Rippin G, Schenk P, Findlay G, Wurst W, Hafner D, Lewis JF, Seeger W, Gunther A, Spragg RG. A Search for subgroups of patients with ARDS who may benefit from surfactant replacement therapy: a pooled analysis of five studies with recombinant surfactant protein-C surfactant (Venticute). Chest 2008, 134:724-732. 10.1378/chest.08-0362, 18689599.
11. Thompson BT. Glucocorticoids and acute lung injury. Crit Care Med 2003, 31(4 Suppl):S253-257.
12. Bernard G, Wheeler A, Naum C, Morris P, Nelson L, Schein R. A placebo controlled, randomised trail of IL-10 in acute lung injury (ALI). Chest 1999, 116(Suppl):260S.
13. Presneill JJ, Harris T, Stewart AG, Cade JF, Wilson JW. A randomized phase II trial of granulocyte-macrophage colony-stimulating factor therapy in severe sepsis with respiratory dysfunction. Am J Resp Crit Care Med 2002, 166:138-143. 10.1164/rccm.2009005, 12119223.
14. Wiedemann HP, Wheeler AP, Bernard GR, Thompson BT, Hayden D, deBoisblanc B, Connors AF, Hite RD, Harabin AL. Comparison of two fluidmanagement strategies in acute lung injury. N Engl J Med 2006, 354:2564-2575.
15. Abroug F, Ouanes-Besbes L, Elatrous S, Brochard L. The effect of prone positioning in acute respiratory distress syndrome or acute lung injury: a meta-analysis. Areas of uncertainty and recommendations for research. Intensive Care Med 2008, 34:1002-1011. 10.1007/s00134-008-1062-3, 18350271.
16. Sud S, Friedrich JO, Taccone P, Polli F, Adhikari NK, Latini R, Pesenti A, Guerin C, Mancebo J, Curley MA, Fernandez R, Chan MC, Beuret P, Voggenreiter G, Sud M, Tognoni G, Gattinoni L. Prone ventilation reduces mortality in patients with acute respiratory failure and severe hypoxemia: systematic review and meta-analysis. Intensive Care Med 2010, 36:585-599. 10.1007/s00134-009-1748-1, 20130832.
17. Erickson SE, Martin GS, Davis JL, Matthay MA, Eisner MD. Recent trends in acute lung injury mortality: 1996-2005. Crit Care Med 2009, 37:1574-1579. 10.1097/CCM.0b013e31819fefdf, 2696257, 19325464.
18. Weiss DJ, Kolls JK, Ortiz L, Panoskaltsis-Mortari A, Prockop DJ. Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 2008, 5:637-667. 10.1513/pats.200804-037DW, 2645238, 18625757.
19. Sueblinvong V, Weiss DJ. Cell therapy approaches for lung diseases: current status. Curr Opin Pharmacol 2009, 9:268-273. 10.1016/j.coph.2009.03.002, 19349209.
20. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000, 342:1334-1349. 10.1056/NEJM200005043421806, 10793167.
21. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, Tetta C, Camussi G. Mesenchymal stem cellderived microvesicles protect against acute tubular injury. J Am Soc Nephrol 2009, 20:1053-1067. 10.1681/ASN.2008070798, 2676194, 19389847.
22. Gatti S, Bruno S, Deregibus MC, Sordi A, Cantaluppi V, Tetta C, Camussi G. Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury. Nephrol Dial Transplant 2011, 26:1474-1483. 10.1093/ndt/gfr015, 21324974.
23. Kanazawa H, Fujimoto Y, Teratani T, Iwasaki J, Kasahara N, Negishi K, Tsuruyama T, Uemoto S, Kobayashi E. Bone marrow-derived mesenchymal stem cells ameliorate hepatic ischemia reperfusion injury in a rat model. PLoS One 2011, 6:e19195. 10.1371/journal.pone.0019195, 3084802, 21559442.
24. Kharaziha P, Hellstrom PM, Noorinayer B, Farzaneh F, Aghajani K, Jafari F, Telkabadi M, Atashi A, Honardoost M, Zali MR, Soleimani M. Improvement of liver function in liver cirrhosis patients after autologous mesenchymal stem cell injection: a phase I-II clinical trial. Eur J Gastroenterol Hepatol 2009, 21:1199-1205. 10.1097/MEG.0b013e32832a1f6c, 19455046.
25. Hare JM, Chaparro SV. Cardiac regeneration and stem cell therapy. Curr Opin Organ Transplant 2008, 13:536-542. 10.1097/MOT.0b013e32830fdfc4, 19060539.
26. Eisner MD, Thompson T, Hudson LD, Luce JM, Hayden D, Schoenfeld D, Matthay MA. Efficacy of low tidal volume ventilation in patients with different clinical risk factors for acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 2001, 164:231-236.
27. Doyle RL, Szaflarski N, Modin GW, Wiener-Kronish JP, Matthay MA. Identification of patients with acute lung injury. Predictors of mortality. Am J Respir Crit Care Med 1995, 152:1818-1824.
28. Mei SHJ, Haitsma JJ, Dos Santos CC, Deng Y, Lai PFH, Slutsky AS, Liles WC, Stewart DJ. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 2010, 182:1047-1057. 10.1164/rccm.201001-0010OC, 20558630.
29. Krasnodembskaya A, Song Y, Fang X, Gupta N, Serikov V, Lee J-W, Matthay M. Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem cells 2010, 28:2229-2238. 10.1002/stem.544, 3293245, 20945332.
30. Chapel A, Bertho JM, Bensidhoum M, Fouillard L, Young RG, Frick J, Demarquay C, Cuvelier F, Mathieu E, Trompier F, Dudoignon N, Germain C, Mazurier C, Aigueperse J, Borneman J, Gorin NC, Gourmelon P, Thierry D. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med 2003, 5:1028-1038. 10.1002/jgm.452, 14661178.
31. Mei SHJ, 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-e269. 10.1371/journal.pmed.0040269, 1961632, 17803352.
32. MacLoughlin RJ, Higgins BD, Laffey JG, O'Brien T. Optimized aerosol delivery to a mechanically ventilated rodent. J Aerosol Med Pulm Drug Deliv 2009, 22:323-332. 10.1089/jamp.2008.0717, 19415985.
33. Lee JW, Fang X, Gupta N, Serikov V, Matthay M. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci USA 2009, 106:16357-16362. 10.1073/pnas.0907996106, 2735560, 19721001.
34. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel RA. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2007, 104:4449-4454. 10.1073/pnas.0700052104, 1838621, 17360544.
35. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147. 10.1126/science.284.5411.143, 10102814.
36. Eguchi G, Kodama R. Transdifferentiation. Curr Opin Cell Biol 1993, 5:1023-1028. 10.1016/0955-0674(93)90087-7, 8129939.
37. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001, 105:369-377. 10.1016/S0092-8674(01)00328-2, 11348593.
38. Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, Fine A. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 2001, 128:5181-5188.
39. Suratt BT, Cool CD, Serls AE, Chen L, Varella-Garcia M, Shpall EJ, Brown KK, Worthen GS. Human pulmonary chimerism after hematopoietic stem cell transplantation. Am J Respir Crit Care Med 2003, 168:318-322. 10.1164/rccm.200301-145OC, 12724127.
40. 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, 179:1855-1863.
41. Ortiz L, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007, 104:11002-11007. 10.1073/pnas.0704421104, 1891813, 17569781.
42. Neuss S, Becher E, Woltje M, Tietze L, Jahnen-Dechent W. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells 2004, 22:405-414. 10.1634/stemcells.22-3-405, 15153617.
43. 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, 285:26211-26222. 10.1074/jbc.M110.119917, 2924032, 20554518.
44. Németh K, Leelahavanichkul A, Yuen PST, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star R, 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, 15:42-49. 10.1038/nm.1905, 2706487, 19098906.
45. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, Pennesi G. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 2005, 35:1482-1490. 10.1002/eji.200425405, 15827960.
46. Danchuk S, Ylostalo JH, Hossain F, Sorge R, Ramsey A, Bonvillain RW, Lasky JA, Bunnell BA, Welsh DA, Prockop DJ, Sullivan DE. Human multipotent stromal cells attenuate lipopolysaccharide-induced acute lung injury in mice via secretion of tumor necrosis factor-alpha-induced protein 6. Stem Cell Res Ther 2011, 2:27. 10.1186/scrt68, 3218818, 21569482.
47. Matthay M, Thompson BT, Read EJ, McKenna DH, Liu KD, Calfee CS, Lee JW. Therapeutic potential of mesenchymal stem cells for severe acute lung injury. Chest 2010, 138:965-972. 10.1378/chest.10-0518, 2951759, 20923800.
48. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976, 4:267-274.
49. Moodley Y, Manuelpillai U, Weiss DJ. Cellular therapies for lung disease: a distant horizon. Respirology 2011, 16(2):223-237. 10.1111/j.1440-1843.2010.01914.x, 21199158.
50. Ortiz L, 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, 100:8407-8411. 10.1073/pnas.1432929100, 166242, 12815096.
51. 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, 180:1131-1142. 10.1164/rccm.200902-0179OC, 3269236, 19713449.
52. 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, 180:1122-1130. 10.1164/rccm.200902-0242OC, 2784417, 19713447.
53. Curley GF, Hayes M, Ansari B, Shaw G, Ryan A, Barry F, O'Brien T, O'Toole D, Laffey JG. Mesenchymal stem cells enhance recovery and repair following ventilator-induced lung injury in the rat. Thorax 2011, [Epub ahead of print].
54. Curley GF, Contreras M, Higgins B, O'Kane C, McAuley DF, O'Toole D, Laffey JG. Evolution of the inflammatory and fibroproliferative responses during resolution and repair following ventilator-induced lung injury in the rat. Anesthesiology 2011, 115:1022-1032. 10.1097/ALN.0b013e31823422c9, 21952251.
55. Xu J, Woods CR, Mora AL, Joodi R, Brigham KL, Iyer S, Rojas M. Prevention of endotoxin-induced systemic response by bone marrow-derived mesenchymal stem cells in mice. Am J Physiol Lung Cell Mol Physiol 2007, 293:L131-141. 10.1152/ajplung.00431.2006, 17416739.
56. Mao M, Wang S-N, Lv X-J, Wang Y, Xu J-C. Intravenous delivery of bone marrow-derived endothelial progenitor cells improves survival and attenuates lipopolysaccharide-induced lung injury in rats. Shock 2010, 34:196-204. 10.1097/SHK.0b013e3181d49457, 20090567.
57. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006, 12:459-465. 10.1038/nm1391, 16582917.
58. Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci USA 2006, 103:17438-17443. 10.1073/pnas.0608249103, 1634835, 17088535.
59. Parekkadan B, van Poll D, Suganuma K, Carter EA, Berthiaume F, Tilles AW, Yarmush ML. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS One 2007, 2:e941. 10.1371/journal.pone.0000941, 1978513, 17895982.
60. Togel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol 2005, 289:F31-42. 10.1152/ajprenal.00007.2005, 15713913.
61. Lee JW, Fang X, Gupta N, Serikov V, Matthay MA. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci USA 2009, 106:16357-16362. 10.1073/pnas.0907996106, 2735560, 19721001.
62. Kursova LV, Konoplyannikov AG, Pasov VV, Ivanova IN, Poluektova MV, Konoplyannikova OA. Possibilities for the use of autologous mesenchymal stem cells in the therapy of radiation-induced lung injuries. Bull Exp Biol Med 2009, 147:542-546. 10.1007/s10517-009-0538-7, 19704968.
63. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, Hermiller JB, Reisman MA, Schaer GL, Sherman W. A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 2009, 54:2277-2286. 10.1016/j.jacc.2009.06.055, 19958962.
64. Falanga V, Iwamoto S, Chartier M, Yufit T, Butmarc J, Kouttab N, Shrayer D, Carson P. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 2007, 13:1299-1312. 10.1089/ten.2006.0278, 17518741.
65. McFarlin K, Gao X, Liu YB, Dulchavsky DS, Kwon D, Arbab AS, Bansal M, Li Y, Chopp M, Dulchavsky SA, Gautam SC. Bone marrow-derived mesenchymal stromal cells accelerate wound healing in the rat. Wound Repair Regen 2006, 14:471-478. 10.1111/j.1743-6109.2006.00153.x, 16939576.
66. Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem cells 2007, 25:2648-2659. 10.1634/stemcells.2007-0226, 17615264.
67. Griffin MD, Ritter T, Mahon BP. Immunological aspects of allogeneic mesenchymal stem cell therapies. Hum Gene Ther 2010, 21:1641-1655. 10.1089/hum.2010.156, 20718666.
68. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, Bundoc VG, Hodges MG, Jelinek I, Madala S, Karpati S, Mezey E. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci USA 2010, 107:5652-5657. 10.1073/pnas.0910720107, 2851758, 20231466.
69. Meisel R, Brockers S, Heseler K, Degistirici O, Bulle H, Woite C, Stuhlsatz S, Schwippert W, Jager M, Sorg R, Henschler R, Seissler J, Dilloo D, Daubener W. Human but not murine multipotent mesenchymal stromal cells exhibit broad-spectrum antimicrobial effector function mediated by indoleamine 2,3-dioxygenase. Leukemia 2011, 25:648-654. 10.1038/leu.2010.310, 21242993.
70. Smith JR, Pochampally R, Perry A, Hsu SC, Prockop DJ. Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem cells 2004, 22:823-831. 10.1634/stemcells.22-5-823, 15342946.
71. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317. 10.1080/14653240600855905, 16923606.
72. Ahrlund-Richter L, De Luca M, Marshak DR, Munsie M, Veiga A, Rao M. Isolation and production of cells suitable for human therapy: challenges ahead. Cell Stem Cell 2009, 4:20-26. 10.1016/j.stem.2008.11.012, 19058776.
73. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007, 110:3499-3506. 10.1182/blood-2007-02-069716, 17664353.
74. Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 2006, 108:2114-2120. 10.1182/blood-2005-11-011650, 1895546, 16690970.
75. Rehman J, Li J, Orschell CM, March KL. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 2003, 107:1164-1169. 10.1161/01.CIR.0000058702.69484.A0, 12615796.
76. Lam C-F, Liu Y-C, Hsu J-K, Yeh P-A, Su T-Y, Huang C-C, Lin M-W, Wu P-C, Chang P-J, Tsai Y-C. Autologous transplantation of endothelial progenitor cells attenuates acute lung injury in rabbits. Anesthesiology 2008, 108:392-401. 10.1097/ALN.0b013e318164ca64, 18292677.
77. Burnham EL, Taylor WR, Quyyumi A, Rojas M, Brigham KL, Moss M. Increased circulating endothelial progenitor cells are associated with survival in acute lung injury. Am J Respir Crit Care Med 2005, 172:854-860. 10.1164/rccm.200410-1325OC, 15976374.
78. Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol 2004, 172:1266-1272.
79. Zhu JH, Wang XX, Zhang FR, Shang YP, Tao QM, Zhu JH, Chen JZ. Safety and efficacy of autologous endothelial progenitor cells transplantation in children with idiopathic pulmonary arterial hypertension: open-label pilot study. Pediatr Transplant 2008, 12:650-655. 10.1111/j.1399-3046.2007.00863.x, 18466198.
80. Wang X-X, Zhang F-R, Shang Y-P, Zhu J-H, Xie X-D, Tao Q-M, Zhu J-H, Chen J-Z. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. J Am Coll Cardiol 2007, 49:1566-1571. 10.1016/j.jacc.2006.12.037, 17418297.
81. Hemmen K, Reinl T, Buttler K, Behler F, Dieken H, Jansch L, Wilting J, Weich HA. High-resolution mass spectrometric analysis of the secretome from mouse lung endothelial progenitor cells. Angiogenesis 2011, 14:163-172. 10.1007/s10456-011-9200-x, 21234671.
82. Hristov M, Erl W, Weber PC. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 2003, 23:1185-1189. 10.1161/01.ATV.0000073832.49290.B5, 12714439.
83. Roszell B, Mondrinos MJ, Seaton A, Simons DM, Koutzaki SH, Fong GH, Lelkes PI, Finck CM. Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 2009, 15(11):3351-3365. 10.1089/ten.tea.2008.0664, 2811058, 19388834.
84. Wang D, Haviland DL, Burns AR, Zsigmond E, Wetsel R. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2007, 104:4449-4454. 10.1073/pnas.0700052104, 1838621, 17360544.
85. Roszell B, Mondrinos MJ, Seaton A, Simons DM, Koutzaki SH, Fong GH, Lelkes PI, Finck CM. Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 2009, 15(11):3351-3365. 10.1089/ten.tea.2008.0664, 2811058, 19388834.
86. Van Vranken BE, Romanska HM, Polak JM, Rippon HJ, Shannon JM, Bishop AE. Coculture of embryonic stem cells with pulmonary mesenchyme: a microenvironment that promotes differentiation of pulmonary epithelium. Tissue Eng 2005, 11(7-8):1177-1187. 10.1089/ten.2005.11.1177, 16144454.
87. Rippon HJ, Lane S, Qin M, Ismail NS, Wilson MR, Takata M, Bishop AE. Embryonic stem cells as a source of pulmonary epithelium in vitro and in vivo. Proc Am Thorac Soc 2008, 5:717-722. 10.1513/pats.200801-008AW, 2643225, 18684724.
88. Wang D, Morales JE, Calame DG, Alcorn JL, Wetsel RA. Transplantation of human embryonic stem cell-derived alveolar epithelial type II cells abrogates acute lung injury in mice. Mol Ther 2010, 18:625-634. 10.1038/mt.2009.317, 2839438, 20087316.
89. Toya SP, Li F, Bonini MG, Gomez I, Mao M, Bachmaier KW, Malik AB. Interaction of a specific population of human embryonic stem cell-derived progenitor cells with CD11b+ cells ameliorates sepsis-induced lung inflammatory injury. Am J Path 2011, 178:313-324. 10.1016/j.ajpath.2010.09.041, 3069906, 21224068.
90. Blum B, Benvenisty N. The tumorigenicity of human embryonic stem cells. Adv Cancer Res 2008, 100:133-158.
91. English K, Wood KJ. Immunogenicity of embryonic stem cell-derived progenitors after transplantation. Curr Opin Organ Transplant 2010, [Epub ahead of print].
92. Magatti M, De Munari S, Vertua E, Gibelli L, Wengler GS, Parolini O. Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem cells 2008, 26:182-192. 10.1634/stemcells.2007-0491, 17901399.
93. Dua HS, Gomes JAP, King AJ, Maharajan VS. The amniotic membrane in ophthalmology. Surv Ophthalmol 2004, 49:51-77. 10.1016/j.survophthal.2003.10.004, 14711440.
94. Moodley Y, Atienza D, Manuelpillai U, Samuel CS, Tchongue J, Ilancheran S, Boyd R, Trounson A. Human umbilical cord mesenchymal stem cells reduce fibrosis of bleomycin-induced lung injury. Am J Pathol 2009, 175:303-313. 10.2353/ajpath.2009.080629, 2708816, 19497992.
95. Alipio ZA, Jones N, Liao W, Yang J, Kulkarni S, Sree Kumar K, Hauer-Jensen M, Ward DC, Ma Y, Fink LM. Epithelial to mesenchymal transition (EMT) induced by bleomycin or TFG(b1)/EGF in murine induced pluripotent stem cell-derived alveolar Type II-like cells. Differentiation 2011, 82:89-98. 10.1016/j.diff.2011.05.001, 21596473.
96. Osafune K, Caron L, Borowiak M, Martinez RJ, Fitz-Gerald CS, Sato Y, Cowan C, Chien KR, Melton DA. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 2008, 26:313-315. 10.1038/nbt1383, 18278034.
97. Nishikawa S-I, Goldstein RA, Nierras CR. The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol 2008, 9:725-729. 10.1038/nrm2466, 18698329.
98. Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM, Stripp BR. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci USA 2009, 106:9286-9291. 10.1073/pnas.0900668106, 2687999, 19478060.
99. Kajstura J, Rota M, R HS, Hosoda T, Sanada F, Zheng H, Ogorek B, Rondonclavo C, Ferreira-martins J, Matsuda A, Arranto C, Goichberg P, Giordano G, Haley KJ, Bardelli S, Rayatzadeh H, Liu X, Quaini F, Liao R, Leri A, Perrella MA, Loscalzo J, Anversa P. Evidence for human lung stem cells. N Engl J Med 2011, 364:1795-1806. 10.1056/NEJMoa1101324, 3197695, 21561345.
100. Chapman HA. Toward lung regeneration. N Engl J Med 2011, 364:1867-1868. 10.1056/NEJMe1101800, 21561353.
101. Hayes M, Curley GF, Laffey JG. Lung stem cells - from an evolving understanding to a paradigm shift?. Stem Cell Res Ther 2011, 2:41. 10.1186/scrt82, 22017959.
102. Chapman HA, Li X, Alexander JP, Brumwell A, Lorizio W, Tan K, Sonnenberg A, Wei Y, Vu TH. Integrin alpha6beta4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Invest 2011, 121:2855-2862. 10.1172/JCI57673, 3223845, 21701069.
103. Hegab AE, Ha VL, Gilbert JL, Zhang KX, Malkoski SP, Chon AT, Darmawan DO, Bisht B, Ooi AT, Pellegrini M, Nickerson DW, Gomperts BN. Novel stem/progenitor cell population from murine tracheal submucosal gland ducts with multipotent regenerative potential. Stem Cells 2011, 29:1283-1293. 10.1002/stem.680, 21710468.
104. Griffiths MJ, Bonnet D, Janes SM. Stem cells of the alveolar epithelium. Lancet 2005, 366:249-260. 10.1016/S0140-6736(05)66916-4, 16023517.
105. Rawlins EL, Hogan BL. Epithelial stem cells of the lung: privileged few or opportunities for many?. Development 2006, 133:2455-2465. 10.1242/dev.02407, 16735479.
106. Chun YS, Chaudhari P, Jang YY. Applications of patient-specific induced pluripotent stem cells; focused on disease modeling, drug screening and therapeutic potentials for liver disease. Int J Biol Sci 2010, 6:796-805. 3005346, 21179587.