Concise review: Current status of stem cells and regenerative medicine in lung biology and diseases

Stem Cells

Volumn 32, Issue 1, 2014, Pages 16-25

  Weiss, Daniel J ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Bioengineering; Cell therapy; Embryonic stem cell; Endogenous progenitor cell; Endothelial progenitor cell; Induced pluripotent stem cell; Lung; Lung diseases; Lung regeneration; Mesenchymal stem cell

Indexed keywords

ASTHMA; BIOENGINEERING; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL TRIAL (TOPIC); EMBRYONIC STEM CELL; EMPHYSEMA; ENDOTHELIAL PROGENITOR CELL; EX VIVO STUDY; HUMAN; IMMUNOMODULATION; LUNG ALVEOLUS EPITHELIUM; LUNG BLOOD VESSEL; LUNG DISEASE; MESENCHYMAL STEM CELL; MORBIDITY; MORTALITY; NONHUMAN; PLURIPOTENT STEM CELL; PREVALENCE; PULMONARY HYPERTENSION; REGENERATIVE MEDICINE; RESPIRATORY AIRFLOW; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

BIOENGINEERING; CELL THERAPY; EMBRYONIC STEM CELL; ENDOGENOUS PROGENITOR CELL; ENDOTHELIAL PROGENITOR CELL; INDUCED PLURIPOTENT STEM CELL; LUNG; LUNG DISEASES; LUNG REGENERATION; MESENCHYMAL STEM CELL;

ANIMALS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LUNG DISEASES; MESENCHYMAL STROMAL CELLS; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TRANSPLANTATION, HOMOLOGOUS;

EID: 84891800634     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1506     Document Type: Review

References (118)

1. Weiss DJ, Bertoncello I, Borok Z et al. Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 2011; 8:223-272.
2. Kassmer SH, Krause DS. Detection of bone marrow-derived lung epithelial cells. Exp Hematol 2010;38:564-573.
3. Sueblinvong V, Loi R, Eisenhauer PL et al. Derivation of lung epithelium from human cord blood-derived mesenchymal stem cells. Am J Respir Crit Care Med 2008; 177:701-711.
4. Loi R, Beckett T, Goncz KK et al. Limited restoration of cystic fibrosis lung epithelium in vivo with adult bone marrow-derived cells. Am J Respir Crit Care Med 2006;173:171-179.
5. Kassmer SH, Bruscia EM, Zhang PX et al. Nonhematopoietic cells are the primary source of bone marrow-derived lung epithelial cells. Stem Cells 2012;30:491-499.
6. De Paepe ME, Mao Q, Ghanta S et al. Alveolar epithelial cell therapy with human cord blood-derived hematopoietic progenitor cells. Am J Path 2011;178:1329-1339.
7. Wong AP, Keating A, Lu WY et al. Identification of a bone marrow-derived epitheliallike population capable of repopulating injured mouse airway epithelium. J Clin Inv 2009;119:336-348.
8. Kotton DN, Fabian AJ, Mulligan RC. Failure of bone marrow to reconstitute lung epithelium. Am J Respir Cell Mol Biol 2005;33: 328-334.
9. Samadikuchaksaraei A, Cohen S, Isaac K et al. Derivation of distal airway epithelium from human embryonic stem cells. Tissue Eng 2006;12:867-875.
10. Wang D, Haviland DL, Burns AR et al. A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc Nat Acad Sci USA 2007;104: 4449-4454.
11. Coraux C, Nawrocki-Raby B, Hinnrasky J et al. Embryonic stem cells generate airway epithelial tissue. Am J Respir Cell Mol Biol 2005;32:87-92.
12. Van Haute L, De Block G, Liebaers I et al. Generation of lung epithelial-like tissue from human embryonic stem cells. Resp Res 2009;10:105.
13. Roszell B, Mondrinos MJ, Seaton A et al. Efficient derivation of alveolar type II cells from embryonic stem cells for in vivo application. Tissue Eng Part A 2009;15:3351-3365.
14. Green MD, Chen A, Nostro MC et al. Generation of anterior foregut endoderm from human embryonic and induced pluripotent stem cells. Nat Biotechnol 2011;29:267-272.
15. Longmire TA, Ikonomou L, Hawkins F et al. Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 2012;10:398-411.
16. Mou H, Zhao R, Sherwood R et al. Generation of multipotent lung and airway progenitors from mouse ESCs and patientspecific cystic fibrosis iPSCs. Cell Stem Cell 2012;10:385-397.
17. Wong AP, Bear CE, Chin S et al. Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein. Nat Biotechnol 2012;30:876-882.
18. Pickering SJ, Minger SL, Patel M et al. Generation of a human embryonic stem cell line encoding the cystic fibrosis mutation deltaF508, using preimplantation genetic diagnosis. Reprod Biomed Online 2005;10:390-397.
19. Somers A, Jean JC, Sommer CA et al. Generation of transgene-free lung diseasespecific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells 2010;28:1728-1740.
20. Kotton DN. Next generation regeneration: The hope and hype of lung stem cell research. Am J Respir Crit Care Med 2012;12: 1255-1260.
21. Rock JR, Hogan BL. Epithelial progenitor cells in lung development, maintenance, repair, and disease. Ann Rev Cell Dev Biol 2011;27:493-512.
22. McQualter JL, Bertoncello I. Concise review: Deconstructing the lung to reveal its regenerative potential. Stem Cells 2012;30: 811-816.
23. Rackley CR, Stripp BR. Building and maintaining the epithelium of the lung. J Clin Inv 2012;122:2724-2730.
24. Driscoll B, Kikuchi A, Lau AN et al. Isolation and characterization of distal lung progenitor cells. Methods Mol Biol 2012;879: 109-122.
25. Reynolds SJ, Brechbul HM, Smith KS et al. Lung epithelial healing: A modified seed and soil concept. Proc Am Thorac Soc 2012;9:27-37.
26. Rock J, Konigshoff M. Endogenous lung regeneration: Potential and limitations. Am J Respir Crit Care Med 2012;186:1213-1219.
27. Rawlins EL, Hogan BL. Epithelial stem cells of the lung: Privileged few or opportunities for many? Development 2006;133:2455-2465.
28. Borthwick DW, Shahbazian M, Krantz QT et al. Evidence for stem-cell niches in the tracheal epithelium. Am J Respir Cell Mol Biol 2001;24:662-670.
29. Anversa P, Kajstura J, Leri A et al. Tissuespecific adult stem cells in the human lung. Nat Med 2011;17:1038-1039.
30. Dobbs LG, Johnson MD, Vanderbilt J et al. The great big alveolar TI cell: Evolving concepts and paradigms. Cell Physiol Biochem 2010;25:55-62.
31. Kim CF, Jackson EL, Woolfenden AE et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 2005;121:823-835.
32. Cole BB, Smith RW, Jenkins KM et al. Tracheal basal cells: A facultative progenitor cell pool. Am J Pathol 2010;177:362-376.
33. Hong KU, Reynolds SD, Giangreco A et al. Clara cell secretory protein-expressing cells of the airway neuroepithelial body microenvironment include a label-retaining subset and are critical for epithelial renewal after progenitor cell depletion. Am J Respir Cell Mol Biol 2001;24:671-681.
34. Rock JR, Randell SH, Hogan BL. Airway basal stem cells: A perspective on their roles in epithelial homeostasis and remodeling. Dis Models Mech 2010;3:545-556.
35. Ghosh M, Brechbuhl HM, Smith RW et al. Context-dependent differentiation of multipotential keratin 14-expressing tracheal basal cells. Am J Respir Cell Mol Biol 2011; 45:403-410.
36. Hegab AE, Ha VL, Darmawan DO et al. Isolation and in vitro characterization of basal and submucosal gland duct stem/progenitor cells from human proximal airways. Stem Cells Trans Med 2012;1:719-724.
37. Perl AK, Wert SE, Loudy DE et al. Conditional recombination reveals distinct subsets of epithelial cells in trachea, bronchi, and alveoli. Am J Respir Cell Mol Biol 2005;33: 455-462.
38. Giangreco A, Arwert EN, Rosewell IR et al. Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci USA 2009;106:9286-9291.
39. Giangreco A, Reynolds SD, Stripp BR. Terminal bronchioles harbor a unique airway stem cell population that localizes to the bronchoalveolar duct junction. Am J Pathol 2002;161:173-182.
40. Teisanu RM, Chen H, Matsumoto K et al. Functional analysis of two distinct bronchiolar progenitors during lung injury and repair. Am J Respir Cell Mol Biol 2011; 44:794-803.
41. Chapman HA, Li X, Alexander JP et al. Integrin b6a4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Invest 2011;121: 2855-2862.
42. Kumar PA, Hu Y, Yamamoto Y et al. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 2011;47:525-538.
43. Chen H, Matsumoto K, Brockway BL et al. Airway epithelial progenitors are region specific and show differential responses to bleomycin-induced lung injury. Stem Cells 2012;30:1948-1960.
44. Volckaert T, Dill E, Campbell A et al. Parabronchial smooth muscle constitutes an airway epithelial stem cell niche in the mouse lung after injury. J Clin Invest 2011;121: 4409-4419.
45. Buckley S, Shi W, Carraro G et al. The milieu of damaged alveolar epithelial type 2 cells stimulates alveolar wound repair by endogenous and exogenous progenitors. Am J Physiol Lung Cell Mol Physiol 2011;45: 1212-1221.
46. Giangreco A, Groot KR, Janes SM. Lung cancer and lung stem cells: Strange bedfellows? Am J Respir Crit Care Med 2007;175: 547-553.
47. Alison MR, Lebrenne AC, Islam S. Stem cells and lung cancer: Future therapeutic targets? Expert Opin Biol Ther 2009;9:1127-1141.
48. Direkze NC, Hodivala-Dilke K, Jeffery R et al. Bone marrow contribution to tumorassociated myofibroblasts and fibroblasts. Cancer Res 2004;64:8492-8495.
49. Hilbe W, Dirnhofer S, Oberwasserlechner F et al. CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer. J Clin Pathol 2004;57:965-969.
50. Arap W, Pasqualini R. Engineered embryonic endothelial progenitor cells as therapeutic Trojan horses. Cancer Cell 2004;5:406-408.
51. Loebinger MR, Janes SM. Stem cells as vectors for antitumour therapy. Thorax 2010; 65:362-369.
52. Wei J, Blum S, Unger M et al. Embryonic endothelial progenitor cells armed with a suicide gene target hypoxic lung metastases after intravenous delivery. Cancer Cell 2004; 5:477-488.
53. Matsuzuka T, Rachakatla RS, Doi C et al. Human umbilical cord matrix-derived stem cells expressing interferon-beta gene significantly attenuate bronchioloalveolar carcinoma xenografts in SCID mice. Lung Cancer 2010;70:28-36.
54. Gomperts BN, Strieter RM. Fibrocytes in lung disease. J Leukoc Biol 2007;82:449-456.
55. Moore BB, Murray L, Das A et al. The role of CCL12 in the recruitment of fibrocytes and lung fibrosis. Am J Respir Cell Mol Biol 2006;35:175-181.
56. Fujiwara A, Kobayashi H, Masuya M et al. Correlation between circulating fibrocytes, and activity and progression of interstitial lung diseases. Respirology 2012;17:693-698.
57. Quesnel C, Piednoir P, Gelly J et al. Alveolar fibrocyte percentage is an independent predictor of poor outcome in patients with acute lung injury. Crit Care Med 2012;40:21-28.
58. Yeager ME, Nguyen CM, Belchenko DD et al. Circulating fibrocytes are increased in children and young adults with pulmonary hypertension. Eur Resp J 2012;39:104-111.
59. LaPar DJ, Burdick MD, Emaminia A et al. Circulating fibrocytes correlate with bronchiolitis obliterans syndrome development after lung transplantation: A novel clinical biomarker. Ann Thorac Surg 2011;92:470-477.
60. Ishii G, Ito TK, Aoyagi K et al. Presence of human circulating progenitor cells for cancer stromal fibroblasts in the blood of lung cancer patients. Stem Cells 2007;25:1469-1477.
61. Asosingh K, Swaidani S, Aronica M et al. Th1-and Th2-dependent endothelial progenitor cell recruitment and angiogenic switch in asthma. J Immunol 2007;178:6482-6494.
62. Fadini GP, Schiavon M, Avogaro A et al. The emerging role of endothelial progenitor cells in pulmonary hypertension and diffuse lung diseases. Sarcoidosis Vasc Diffuse Lung Dis 2007;24:85-93.
63. Burnham EL, Taylor WR, Quyyumi AA et al. Increased circulating endothelial progenitor cells are associated with survival in acute lung injury. Am J Respir Crit Care Med 2005;172:854-860.
64. Palange P, Testa U, Huertas A et al. Circulating haemopoietic and endothelial progenitor cells are decreased in COPD. Eur Respir J 2006;27:529-541.
65. Dome B, Timar J, Dobos J et al. Identification and clinical significance of circulating endothelial progenitor cells in human nonsmall cell lung cancer. Cancer Res 2006;66: 7341-7347.
66. Borghesi A, Massa M, Campanelli R et al. Circulating endothelial progenitor cells in pre-term infants with bronchopulmonary dysplasia. Am J Resp Crit Care Med 2009; 180:540-546.
67. Cribbs SK, Sutcliffe DJ, Taylor WR et al. Circulating endothelial progenitor cells inversely associate with organ dysfunction in sepsis. Intensive Care Med 2012;38:429-436.
68. Huertas A, Palange P. Circulating endothelial progenitor cells and chronic pulmonary diseases. Eur Respir J 2011;37:426-431.
69. Zhao YD, Courtman DW, Deng Y et al. Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrowderived endothelial-like progenitor cells: Efficacy of combined cell and eNOS gene therapy in established disease. Circ Res 2005;96:442-450.
70. Lam C-F, Roan J-N, Lee C-H et al. Transplantation of endothelial progenitor cells improves pulmonary endothelial function and gas exchange in rabbits with endotoxininduced acute lung injury. Anesth Analg 2011;112:620-627.
71. Balasubramaniam V, Ryan SL, Seedorf GJ et al. 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:L315-L323.
72. Lavoie JR, Stewart DJ. Genetically modified endothelial progenitor cells in the therapy of cardiovascular disease and pulmonary hypertension. Curr Vasc Pharmacol 2012;10: 289-299.
73. Stewart DJ, Mei SH. Cell-based therapies for lung vascular diseases: Lessons for the future. Proc Am Thorac Soc 2011;8:535-540.
74. Wang XX, Zhang FR, Shang YP et al. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: A p54. Pilot randomized controlled trial. J Am Coll Cardiol 2007;49:1566-1571.
75. Zhu JH, Wang XX, Zhang FR et al. 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.
76. Keating A. Mesenchymal stromal cells: New directions. Cell Stem Cell 2012;10:709-716.
77. Prockop DJ, Oh JY. Medical therapies with adult stem/progenitor cells (MSCs): A backward journey from dramatic results in vivo to the cellular and molecular explanations. J Cell Biochem 2012;113:1460-1469.
78. Islam MN, Das SR, Emin MT et al. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 2012;8: 759-765.
79. Tropea KA, Leder E, Aslam M et al. 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:L829-L837.
80. Lalu MM, McIntyre L, Pugliese C et al. Safety of cell therapy with mesenchymal stromal cells (Safecell): A systematic review and meta-analysis of clinical trials. PLoS One 2012;7:e47559.
81. Von Bahr L, Batsis I, Moll G et al. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells 2012;30:1575-1578.
82. Matthay MA, Taylor Thompson B, Read EJ et al. Therapeutic potential of mesenchymal stem cells for severe acute lung injury. Chest 2010;138:965-972.
83. O'Reilly M. Thebaud B. Cell-based strategies to reconstitute lung function in infants with severe bronchopulmonary dysplasia. Clin Perinatol 2012;39:703-725.
84. Lee JW, Krasnodembskaya A, McKenna DH et al. Therapeutic effects of human mesenchymal stem cells in ex vivo human lungs injured with live bacteria. Am J Respir Crit Care Med 2013;187:751-760.
85. Kim ES, Chang YS, Choi SJ et al. Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells attenuates Escherichia coli-induced acute lung injury in mice. Resp Res 2011;12:108.
86. Epperly MW, Guo H, Gretton JE et al. Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am J Respir Cell Mol Biol 2003;29:213-224.
87. Yan X, Liu Y, Han Q et al. Injured microenvironment directly guides the differentiation of engrafted Flk-1(1) mesenchymal stem cell in lung. Exp Hematol 2007;35: 1466-1475.
88. Weiss DJ, Rojas M. MSCs in chronic lung diseases: COPD and lung fibrosis. In: Gross G, Häupl T, eds. Stem Cell-Dependent Therapies. Berlin: Walter de Gruyter GmbH & Co, 2013.
89. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54-63.
90. Ionescu L, Byrne RN, van Haaftern T et al. Stem cell conditioned medium improves acute lung injury in mice: In vivo evidence for stem cell paracrine action. Am J Physiol Lung Cell Mol Physiol 2012;303:L967-L977.
91. Goodwin M, Sueblinvong V, Eisenhauer P et al. Bone marrow derived mesenchymal stromal cells inhibit th2-Mediated allergic airways inflammation in mice. Stem Cells 2011; 29:1137-1148.
92. Araujo IM, Abreu SC, Maron-Gutierrez T et al. Bone marrow-derived mononuclear cell therapy in experimental pulmonary and extrapulmonary acute lung injury. Crit Care Med 2010;38:1733-1741.
93. Hodges RJ, Lim R, Jenkin G et al. Amnion epithelial cells as a candidate therapy for acute and chronic lung injury. Stem Cells Int 2012;709:63.
94. Matute-Bello G, Downey G, Moore BB et al. An official American Thoracic Society workshop report: Features and measurements of experimental acute lung injury in animals. Am J Resp Cell Mol Biol 2011;44: 725-738.
95. Weiss DJ, Casaburi R, Flannery R et al. A placebo-controlled randomized trial of mesenchymal stem cells in chronic obstructive pulmonary disease. Chest 2013;143:1590-1598.
96. Toonkel RL, Hare JM, Matthay MA et al. Mesenchymal stem cells and idiopathic pulmonary fibrosis: Potential for clinical testing. Am J Respir Crit Care Med 2013;188:133-140.
97. Weiss DJ, Ortiz LA. Cell therapy trials for lung diseases: Progress and cautions. Am J Resp Crit Care Med 2013;188:123-125.
98. Master Z, Resnik DB. Stem cell tourism and scientific responsibility. Stem-cell tourism and scientific responsibility. Stem-cell researchers are in a unique position to curb the problem of stem-cell tourism. EMBO Rep 2011;12:992-995.
99. Qiu J. Trading on hope. Nat Biotechnol 2010;27:790-92.
100. Zarzeczny A, Rachul C, Nisbet M et al. Stem cell clinics in the news. Nat Biotechnol 2012;28:1243-1246.
101. Badylak SF, Weiss DJ, Caplan A et al. Engineered whole organs and complex tissues. Lancet 2012;379:943-952.
102. Fishman JM, De Coppi P, Elliott MJ et al. Airway tissue engineering. Expert Opin Biol Ther 2011;11:1623-1635.
103. Mondrinos MJ, Koutzaki S, Jiwanmall E et al. Engineering three-dimensional pulmonary tissue constructs. Tissue Eng 2006;12: 717-728.
104. Nichols JE, Cortiella JC. Engineering of a complex organ progress toward development of a tissue-engineered lung. Proc Am Thorac Soc 2008;5:723-730.
105. Panoskaltsis-Mortari A, Weiss DJ. Breathing new life into lung transplantation therapy. Mol Ther 2010;18:1581-1583.
106. Price AP, England KA, Matson AM et al. Development of a decellularized lung bioreactor system for bioengineering the lung: The matrix reloaded. Tissue Eng Part A 2010; 16:2581-2591.
107. Cortiella J, Niles J, Cantu A et al. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng Part A 2010; 16:2565-2580.
108. Petersen TH, Calle EA, Zhao L et al. Tissue-engineered lungs for in vivo implantation. Science 2010;329:538-541.
109. Ott HC, Clippinger B, Conrad C et al. Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 2010;16:927-933.
110. Bonenfant N, Sokocevic D, Wagner DE et al. The effects of storage and sterilization on de-cellularized and re-cellularized whole lung. Biomaterials 2013;34:3231-3245.
111. Bonvillain RW, Danchuk S, Sullivan DE et al. A nonhuman primate model of lung regeneration: Detergent-mediated decellularization and initial in vitro recellularization with mesenchymal stem cells. Tissue Eng Part A 2012;18:2437-2452.
112. Daly AB, Wallis JM, Borg ZD et al. Initial binding and re-cellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng Part A 2012;18:1-16.
113. Jensen T, Roszell B, Zang F et al. A rapid lung de-cellularization protocol supports embryonic stem cell differentiation in vitro and following implantation. Tissue Eng Part C: Methods 2012;18:632-646.
114. Sokocevic D, Bonenfant N, Wagner DE et al. The effect of age and emphysematous and fibrotic injury on the re-cellularization of de-cellularized lungs. Biomaterials 2013;34: 3256-3269.
115. Wallis JM, Borg ZD, Daly AB et al. Comparative assessment of detergent-based protocols for mouse lung de-cellularization and re-cellularization. Tissue Eng Part C: Methods 2012;18:420-432.
116. Nichols JE, Niles JA, Cortiella J. Production and utilization of acellular lung scaffolds in tissue engineering. J Cell Biochem 2012; 113:2185-2192.
117. Huh D, Matthews BD, Mammoto A et al. Reconstituting organ-level lung functions on a chip. Science 2010;328:1662-1668.
118. Huh D, Leslie DC, Matthews BD et al. A human disease model of drug toxicityinduced pulmonary edema in a lung-on-achip microdevice. Sci Transl Med 2012;4:147.