Therapeutic potential of stem cells in lung disease: Progress and pitfalls

Clinical Science

Volumn 114, Issue 1-2, 2008, Pages 99-108

  Loebinger, Michael R ^a   Aguilar, Susana ^a   Janes, Sam M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Airway; Bone marrow; Epithelial cell; Gene therapy; Lung disease; Progenitor; Stem cell

Indexed keywords

CELL THERAPY; EMBRYONIC STEM CELL; ENGRAFTMENT; GENE THERAPY; LUNG DISEASE; LUNG PARENCHYMA; PRIORITY JOURNAL; REVIEW; STEM CELL; TISSUE INJURY; TISSUE REPAIR; CYTOLOGY; HUMAN; METHODOLOGY; RESPIRATORY SYSTEM; STEM CELL TRANSPLANTATION; TRANSPLANTATION;

EMBRYONIC STEM CELLS; GENE THERAPY; HUMANS; LUNG DISEASES; RESPIRATORY SYSTEM; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 38349064863     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20070073     Document Type: Review

References (86)

1. Hind, M. and Maden, M. (2003) Retinoic acid, a regeneration-inducing molecule. Dev. Dyn. 226, 237-244
2. Griffiths, M. J. D., Bonnet, D. and Janes, S. M. (2005) Stem cells of the alveolar epithelium. Lancet 366, 249-260
3. Marshall, R., Bellingan, G. and Laurent, G. (1998) The acute respiratory distress syndrome: fibrosis in the fast lane. Thorax 53, 815-817
4. Engelhardt, J. F. (2001) Stem cell niches in the mouse airway. Am. J. Respir. Cell Mol. Biol. 24, 649-652
5. Otto, W. R. (2002) Lung epithelial stem cells. J. Pathol. 197, 527-535
6. Breuer, R., Zajicek, G., Christensen, T. G., Christensen, T. G., Lucey, E. C. and Snider, G. L. (1990) Cell kinetics of normal adult hamster bronchial epithelium in the steady state. Am. J. Respir. Cell Mol. Biol. 2, 51-58
7. Rawlins, E. L. and Hogan, B. L. M. (2006) Epithelial stem cells of the lung: privileged few or opportunities for many. Development 133, 2455-2465
8. Hong, K. U., Reynolds, S. D., Watkins, S., Fuchs, E. and Stripp, B. R. (2004) Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am. J. Path. 164, 577-588
9. Kim, C. F. B., Jackson, E. L. and Woolfenden, A. E. (2005) Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835
10. Uhal, B. D. (1997) Cell cycle kinetics in the alveolar epithelium. Am. J. Physiol. 272, L1031-L1045
11. Anderson, W. R. and Thielen, K. (1992) Correlative study of adult respiratory distress syndrome by light, scanning, and transmission electron microscopy. Ultrastruct. Pathol. 16, 615-628
12. Majka, S. M., Beutz, M. A., Hagen, M., Izzo, A. A., Voelkel, N. and Helm, K. M. (2005) Identification of novel resident pulmonary stem cells: form and function of the lung side population. Stem Cells 23, 1073-1081
13. Reynolds, S. D., Shen, H., Reynolds, P. R. et al. (2007) Molecular and functional properties of lung side population cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L972-L983
14. Orkin, S. H. and Morrison, S. J. (2002) Biomedicine: stem-cell competition. Nature 418, 25-27
15. Bonnet, D. (2003) Biology of human bone marrow stem cells. Clin. Exp. Med. 3, 140-149
16. Krause, D. S., Theise, N. D., Collector, M. I. et al. (2001) Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105, 369-377
17. Kotton, D. N., Ma, B. Y., Cardoso, W. V. et al. (2001) Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 128, 5181-5188
18. Theise, N. D., Henegariu, O., Grove, J. et al. (2002) Radiation pneumonitis in mice: A severe injury model for pneumocyte engraftment from bone marrow. Exp. Haematol. 30, 1333-1338
19. Anjos-Afonso, F. S. E. and Bonnet, D. (2004) In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci. 117, 5655-5664
20. MacPherson, H., Keir, P., Webb, S. et al. (2005) Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo. J. Cell Sci. 118, 2441-2450
21. Yamada, M., Kubo, H., Kobayashi, S. et al. (2004) Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J. Immunol. 172, 1266-1272
22. Ishizawa, K., Kubo, H., Yamada, M. et al. (2004) Bone marrow-derived cells contribute to lung regeneration after elastase-induced pulmonary emphysema. FEBS Lett. 556, 249-252
23. Hashimoto, N., Jin, H., Liu, T., Chensue, S. W. and Phan, S. H. (2004) Bone marrow-derived progenitor cells in pulmonary fibrosis. J. Clin. Invest. 113, 243-252
24. Ortiz, L. A., Gambelli, F., McBride, C. et al. (2003) Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc. Natl. Acad. Sci. U.S.A. 100, 8407-8411
25. Rojas, M., Xu, J., Woods, C. R. et al. (2005) Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am. J. Respir. Cell Mol. Biol. 33, 145-152
26. Aliotta, J. M., Keaney, P., Passero, M. et al. (2006) Bone marrow production of lung cells: the impact of G-CSF, cardiotoxin, graded doses of irradiation, and subpopulation phenotype. Exp. Haematol. 34, 230-241
27. Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L. et al. (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49
28. 27a Erratum (2007) Nature 447, 879-880
29. Wagers, A., Sherwood, R. I., Christensen, J. L. and Weissman, I. L. (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297, 2256-2259
30. Epperly, M. W., Guo, H., Gretton, J. E. et al. (2003) Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 29, 213-224
31. Direkze, N. C., Forbes, S. J., Brittan, M. et al. (2003) Multiple organ engraftment by bone-marrow-derived myofibroblasts and fibroblasts in bone-marrow-transplanted mice. Stem Cells 21, 514-520
32. Schmidt, M., Sun, G., Stacey, M. A., Mori, L. and Mattoli, S. (2003) Identification of circulating fibrocytes as precursors of bronchial myofibroblasts in asthma. J. Immunol. 170, 380-389
33. Zhao, Y. D., Courtman, D. W., Deng, Y., Kugathasan, L., Zhang, Q. and Stewart, D. J. (2005) Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells. Circ. Res. 96, 442-450
34. Ying, Q. L., Nichols, J. and Evans, E. P. Changing potency by spontaneous fusion. Nature 416, 545-548
35. Herzog, E. L., Chai, L. and Krause, D. S. (2003) Plasticity of marrow-derived stem cells. Blood 102, 3483-3493
36. Wang, X., Willenbring, H., Akkari, Y. et al. (2003) Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422, 897-901
37. Harris, R. G., Herzog, E. L., Bruscia, E. M., Grove, J. E., Van Arnam, J. S. and Krause, D. S. (2004) Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 305, 90-93
38. Kleeberger, W., Versmold, A., Rothamel, T. et al. (2003) Increased chimerism of bronchial and alveolar epithelium in human lung allografts undergoing chronic injury. Am. J. Pathol. 162, 1487-1494
39. Spencer, H., Rampling, D., Aurora, P., Bonnet, D., Hart, S. L. and Jaffé, A. (2005) Transbronchial biopsies provide longitudinal evidence for epithelial chimerism in children following sex mismatched lung transplantation. Thorax 60, 60-62
40. Zander, D. S., Baz, M. A., Cogle, C. R., Visner, G. A., Theise, N. D. and Crawford, J. M. (2005) Bone marrow-derived stem-cell repopulation contributes minimally to the Type II pneumocyte pool in transplanted human lungs. Transplantation 80, 206-212
41. Albera, C., Polak, J. M., Janes, S. et al. (2005) Repopulation of human pulmonary epithelium by bone marrow cells: a potential means to promote repair. Tissue Eng. 11, 1115-1121
42. Suratt, B. T., Cool, C. D., Serls, A. E. et al. (2003) Human pulmonary chimerism after haematopoietic stem cell transplantation. Am. J. Resp. Crit. Care 168, 318-322
43. Mattsson, J., Jansson, M., Wernerson, A. and Hassan, M. (2004) Lung epithelial cells and type II pneumocytes of donor origin after allogeneic hematopoietic stem cell transplantation. Transplantation 78, 154-157
44. Zander, D. S., Cogle, C. R., Theise, N. D. and Crawford, J. M. (2006) Donor-derived type II pneumocytes are rare in the lungs of allogeneic hematopoietic cell transplant recipients. Ann. Clin. Lab. Sci. 36, 47-52
45. Davies, J. C., Potter, M., Bush, A. et al. (2002) Bone marrow stem cells do not repopulate the healthy upper respiratory tract. Pediatr. Pulmonol. 34, 251-256
46. Phillips, R. J., Burdick, M. D., Hong, K. et al. (2004) Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J. Clin. Invest. 114, 438-446
47. Kotton, D. N., Fabian, A. J. and Mulligan, R. C. (2005) Failure of bone marrow to reconstitute lung epithelium. Am. J. Respir. Cell Mol. Biol. 33, 328-334
48. Chang, J. C., Summer, R., Sun, X., Fitzsimmons, K. and Fine, A. (2005) Evidence that bone marrow cells do not contribute to the alveolar epithelium. Am. J. Respir. Cell Mol. Biol. 33, 335-342
49. Aldhous, P., Reich, E. S. (2007) Flawed stem cell data withdrawn. New Scientist 2591, 12
50. Weiss, D. J., Berberich, M. A., Borok, Z. et al. (2006) Adult stem cells, lung biology, and lung disease. Proc. Am. Thorac. Soc. 3, 193-207
51. Krause, D. S. (2005) Engraftment of bone marrow-derived epithelial cells. Ann. N.Y. Acad. Sci. 1044, 117-124
52. Bruscia, E. M., Price, J. E., Cheng, E. C. et al. (2006) Assessment of cystic fibrosis transmembrane conductance regulator (CFTR) activity in CFTR-null mice after bone marrow transplantation. Proc. Natl. Acad. Sci. U.S.A. 103, 2965-2970
53. Bruscia, E. M., Ziegler, E. C., Price, J. E., Weiner, S., Egan, M. E. and Krause, D. S. (2006) Engraftment of donor-derived epithelial cells in multiple organs following bone marrow transplantation into newborn mice. Stem Cells 24, 2299-2308
54. Lunde, K., Solheim, S., Aakhus, S. et al. (2006) Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N. Engl. J. Med. 355, 1199-1209
55. Schachinger, V., Erbs, S., Elsasser, A. et al. (2006) Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 355, 1210-1221
56. Assmus, B., Honold, J., Schachinger, V. et al. (2006) Transcoronary transplantation of progenitor cells after myocardial infarction. N. Engl. J. Med. 355, 1222-1232
57. Rosenzweig, A. (2006) Cardiac cell therapy: mixed results from mixed cells. N. Eng. J. Med. 355, 1274-1277
58. Baum, C., Dullmann, J., Li, Z. et al. (2003) Side effects of retroviral gene transfer into hematopoietic stem cells. Blood 101, 2099-2114
59. Fang, T.-C., Alison, M. R., Wright, N. A. and Poulsom, R. (2004) Adult stem cell plasticity: will engineered tissues be rejected? Int. J. Exp. Pathol. 85, 115-124
60. Grove, J. E., Lutzko, C., Priller, J. et al. (2002) Marrow-derived cells as vehicles for delivery of gene therapy to pulmonary epithelium. Am J Respir Cell Mol Biol. 27, 645-651
61. Lagasse, E., Connors, H., Al-Dhalimy, M. et al. (2000) Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 6, 1229-1234
62. Wang, G., Bunnell, B. A., Painter, R. G. et al. (2005) Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis. Proc. Natl. Acad. Sci. U.S.A. 102, 186-191
63. Loi, R., Beckett, T., Goncz, K. K., Suratt, B. T. and Weiss, D. J. (2006) Limited restoration of cystic fibrosis lung epithelium in vivo with adult bone marrow-derived cells. Am. J. Respir. Crit. Care Med. 173, 171-179
64. Dorin, J. R., Farley, R., Webb, S. et al. (1996) A demonstration using mouse models that successful gene therapy for cystic fibrosis requires only partial gene correction. Gene Ther. 3, 797-801
65. McAnulty, R. J. (2007) Fibroblasts and myofibroblasts: Their source, function and role in disease. Int. J. Biochem. Cell Biol. 39, 666-671
66. Bucala, R., Spiegel, L. A., Chesney, J., Hogan, M. and Cerami, A. (1994) Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol. Med. 1, 71-81
67. Stenmark, K. R., Davie, N. J., Reeves, J. T. and Frid, M. G. (2005) Hypoxia, leucocytes, and the pulmonary circulation. J. Appl. Physiol. 98, 715-721
68. Stenmark, K. R., Fagan, K. A. and Frid, M. G. (2006) Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ. Res. 99, 675-691
69. Jordan, C. T., Guzman, M. L. and Noble, M. (2006) Cancer stem cells. N. Eng. J. Med. 355, 1253-1261
70. Rubio, D., Garcia-Castro, J., Martín, M. C. et al. (2005) Spontaneous human adult stem cell transformation. Cancer Res. 65, 3035-3039
71. Tolar, J., Nauta, A. J. and Osborn, M. J. et al (2007) Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25, 371-379
72. Aguilar, S., Nye, E., Chan, J., et al. (2007) Murine but not human mesenchymal stem cells generate osteosarcoma-like lesions in the lung. Stem Cells 25, 1586-1594
73. Houghton, J., Stoicov, C., Nomura, S. et al. (2004) Gastric cancer originating from bone marrow-derived cells. Science 306, 1568-1571
74. Direkze, N. C., Hodivala-Dilke, K., Jeffery, R. et al. (2004) Bone marrow contribution to tumour associated myofibroblasts and fibroblasts. Cancer Res. 64, 8492-8495
75. Direkze, N. C. and Alison, M. R. (2006) Bone marrow and tumour stroma: an intimate relationship. Haematol. Oncol. 24, 189-195
76. Desmouliere, A., Guyot, C. and Gabbiani, G. (2004) The stroma reaction myofibroblast: a key player in the control of tumor cell behaviour. Int. J. Dev. Biol. 48, 509-517
77. De Wever, O. and Mareel, M. (2003) Role of tissue stroma in cancer cell invasion. J. Pathol. 200, 429-447
78. Zhu, W., Xu, W., Jiang, R. et al. (2006) Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp. Mol. Pathol. 80, 267-274
79. Khakoo, A. Y., Pati, S. and Anderson, S. A. et al (2006) Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J. Exp. Med. 203, 1235-1247
80. Sangai, T., Ishii, G. and Kodama, K. et al (2005) Effect of differences in cancer cells and tumor growth sites on recruiting bone marrow-derived endothelial cells and myofibroblasts in cancer-induced stroma. Int. J. Cancer 115, 885-892
81. Check, E. (2002) Gene therapy: a tragic setback. Nature 420, 116-118
82. Coraux, C., Nawrocki-Raby, B., Hinnrasky, J. et al. (2005) Embryonic stem cells generate airways epithelial tissue. Am. J. Respir. Crit. Care Med. 32, 87-92
83. Ali, N. N., Edgar, A. J., Samadikuchaksaraei, A. et al. (2002) Derivation of type II alveolar epithelial cells from murine embryonic stem cells. Tissue Eng. 8, 541-550
84. Rippon, H. J., Polak, J. M., Qin, M. and Bishop, A. E. (2006) Derivation of distal lung epithelial progenitors from murine embryonic stem cells using a novel three-step differentiation protocol. Stem Cells 24, 1389-1398
85. Wang, D., Haviland, D. L., Burns, A. R., Zsigmond, E. and Wetsel, R. A. (2007) A pure population of lung alveolar epithelial type II cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 104, 4449-4454
86. (2004) No consensus on stem cells. Nature 428, 587