Developing cell therapy techniques for respiratory disease: Intratracheal delivery of genetically engineered stem cells in a murine model of airway injury

Human Gene Therapy

Volumn 20, Issue 11, 2009, Pages 1329-1343

  Leblond, Anne Laure ^a,b   Naud, Patrice ^a,b,c   Forest, Virginie ^a,b   Gourden, Clothilde ^d   Sagan, Christine ^e   Romefort, Bénédicte ^a,b,f   Mathieu, Eva ^a,b   Delorme, Bruno ^a,g   Collin, Christine ^g,h   Pagès, Jean Christophe ^g,h   Sensebé, Luc ^a,g,i   Pitard, Bruno ^a,b   Lemarchand, Patricia ^a,b,f  

^a INSERM   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c CNRS   (France)

^d In Cell Art   (France)

^e NANTES UNIVERSITY HOSPITAL   (France)

^f L INSTITUT DU THORAX   (France)

^g UNIVERSITÉ DE TOURS   (France)

^h UNIVERSITY HOSPITAL OF TOURS   (France)

ⁱ ETABLISSEMENT FRANÇAIS DU SANG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

POLIDOCANOL; 5-BROMO-4-CHLORO-3-INDOLYL BETA-GALACTOSIDE; BETA GALACTOSIDASE; GALACTOSIDE; INDOLE DERIVATIVE; PRIMER DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS; CELL LINE; CELL SURVIVAL; CELL THERAPY; CONTROLLED STUDY; CYSTIC FIBROSIS; EMBRYONIC STEM CELL; ENGRAFTMENT; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL MODEL; EXPERIMENTAL MOUSE; GENE EXPRESSION; GENE THERAPY; GENETIC ENGINEERING; GRAFT SURVIVAL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LUNG; LUNG ALVEOLUS EPITHELIUM; LUNG INJURY; LUNG LAVAGE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REPORTER GENE; RESPIRATORY TRACT DISEASE; STEM CELL GENE THERAPY; TRACHEA; ANALYSIS OF VARIANCE; ANIMAL; BIOLOGICAL THERAPY; CYTOLOGY; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; PROCEDURES; RESPIRATORY TRACT DISEASES; TRANSPLANTATION;

MURINAE;

ANALYSIS OF VARIANCE; ANIMALS; BETA-GALACTOSIDASE; BRONCHOALVEOLAR LAVAGE; CELL- AND TISSUE-BASED THERAPY; DNA PRIMERS; EMBRYONIC STEM CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GALACTOSIDES; GENETIC ENGINEERING; GENETIC VECTORS; INDOLES; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; RESPIRATORY TRACT DISEASES; TRACHEA; TRANSFECTION;

EID: 70449102888     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2009.035     Document Type: Article

References (64)

1. Alton, E.W., Stern, M., Farley, R., Jaffe, A., Chadwick, S.L., Phillips, J., Davies, J., Smith, S.N., Browning, J., Davies, M.G., Hodson, M.E., Durham, S.R., Li, D., Jeffery, P.K., Scallan, M., Balfour, R., Eastman, S.J., Cheng, S.H., Smith, A.E., Meeker, D., and Geddes, D.M. (1999). Cationic lipid-mediated CFTR gene transfer to the lungs and nose of patients with cystic fibrosis: A double-blind placebo-controlled trial. Lancet 353, 947-954.
2. Aluigi, M., Fogli, M., Curti, A., Isidori, A., Gruppioni, E., Chio-doni, C., Colombo, M.P., Versura, P., D'Errico-Grigioni, A., Ferri, E., Baccarani, M., and Lemoli, R.M. (2006). Nucleofection is an efficient nonviral transfection technique for human bone marrow-derived mesenchymal stem cells. Stem Cells 24, 454-461.
3. Arnhold, S., Absenger, Y., Klein, H., Addicks, K., and Schraer-meyer, U. (2007). Transplantation of bone marrow-derived mesenchymal stem cells rescue photoreceptor cells in the dystrophic retina of the rhodopsin knockout mouse. Graefes Arch. Clin. Exp. Ophthalmol. 245, 414-422.
4. Aubert, D., Menoret, S., Chiari, E., Pichard, V., Durand, S., Tesson, L., Moullier, P., Anegon, I., and Ferry, N. (2002). Cy-totoxic immune response blunts long-term transgene expression after efficient retroviral-mediated hepatic gene transfer in rat. Mol. Ther. 5, 388-396.
5. Beckett, T., Loi, R., Prenovitz, R., Poynter, M., Goncz, K.K., Suratt, B.T., and Weiss, D.J. (2005). Acute lung injury with endotoxin or NO2 does not enhance development of airway epithelium from bone marrow. Mol. Ther. 12, 680-686.
6. Borthwick, D.W., Shahbazian, M., Krantz, Q.T., Dorin, J.R., and Randell, S.H. (2001). Evidence for stem-cell niches in the tracheal epithelium. Am. J. Respir. Cell Mol. Biol. 24, 662-670.
7. Bottino, R., Lemarchand, P., Trucco, M., and Giannoukakis, N. (2003). Gene-and cell-based therapeutics for type I diabetes mellitus. Gene Ther. 10, 875-889.
8. 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.
9. Castro, R.F., Jackson, K.A., Goodell, M.A., Robertson, C.S., Liu, H., and Shine, H.D. (2002). Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297, 1299.
10. Chan, J., O'Donoghue, K., de la Fuente, J., Roberts, I.A., Kumar, S., Morgan, J.E., and Fisk, N.M. (2005). Human fetal mesen-chymal stem cells as vehicles for gene delivery. Stem Cells 23, 93-102.
11. Chapelier, A., Danel, C., Mazmanian, M., Bacha, E.A., Sellak, H., Gilbert, M.A., Herve, P., and Lemarchand, P. (1996). Gene therapy in lung transplantation: Feasibility of ex vivo adeno-virus-mediated gene transfer to the graft. Hum. Gene Ther. 7, 1837-1845.
12. Chateauvieux, S., Ichante, J.L., Delorme, B., Frouin, V., Pietu, G., Langonne, A., Gallay, N., Sensebe, L., Martin, M.T., Moore K.A., and Charbord, P. (2007). Molecular profile of mouse stromal mesenchymal stem cells. Physiol. Genomics 29, 128-138.
13. Chidgey, A.P., Layton, D., Trounson, A., and Boyd, R.L. (2008). Tolerance strategies for stem-cell-based therapies. Nature 453, 330-337.
14. Conrad, C., Gupta, R., Mohan, H., Niess, H., Bruns, C.J., Kopp, R., von Luettichau, I., Guba, M., Heeschen, C., Jauch, K.W., Huss, R., and Nelson, P.J. (2007). Genetically engineered stem cells for therapeutic gene delivery. Curr. Gene Ther. 7, 249-260.
15. Coraux, C., Nawrocki-Raby, B., Hinnrasky, J., Kileztky, C., Gaillard, D., Dani C., and Puchelle, E. (2005). Embryonic stem cells generate airway epithelial tissue. Am. J. Respir. Cell Mol. Biol. 32, 87-92.
16. D'Cruz, P.M., Yasumura, D., Weir, J., Matthes, M.T., Abderra-him, H., LaVail, M.M., and Vollrath, D. (2000). Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 9, 645-651.
17. Dennis, J.E., and Caplan, A.I. (1996). Differentiation potential of conditionally immortalized mesenchymal progenitor cells from adult marrow of a H-2K+-tsA58 transgenic mouse. J. Cell Physiol. 167, 523-538.
18. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., and Horwitz, E. (2006). Minimal criteria for defining multi-potent mesenchymal stromal cells: The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317.
19. Driscoll, K.E., Costa, D.L., Hatch, G., Henderson, R., Oberdor-ster, G., Salem, H., and Schlesinger, R.B. (2000). Intratracheal instillation as an exposure technique for the evaluation of respiratory tract toxicity: Uses and limitations. Toxicol. Sci. 55, 24-35.
20. Engelhardt, J.F., Yankaskas, J.R., and Wilson, J.M. (1992). In vivo retroviral gene transfer into human bronchial epithelia of xe-nografts. J. Clin. Invest. 90, 2598-2607.
21. Gupta, N., Su, X., Popov, B., Lee, J.W., Serikov, V., and Matthay, M.A. (2007). Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J. Immunol. 179, 1855-1863.
22. Humphries, M.M., Rancourt, D., Farrar, G.J., Kenna, P., Hazel, M., Bush, R.A., Sieving, P.A., Sheils, D.M., McNally, N., Creighton, P., Erven, A., Boros, A., Gulya, K., Capecchi, M.R., and Humphries, P. (1997). Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet. 15, 216-219.
23. Inoue, Y., Iriyama, A., Ueno, S., Takahashi, H., Kondo, M., Ta-maki, Y., Araie, M., and Yanagi, Y. (2007). Subretinal transplantation of bone marrow mesenchymal stem cells delays retinal degeneration in the RCS rat model of retinal degeneration. Exp. Eye Res. 85, 234-241
24. Institute of Laboratory Animal Research, Commission on Life Sciences, National Research Council. (1996). Guide for the Care and Use of Laboratory Animals. NIH Publication No. 85-123 (National Academies Press, Washington, D.C.).
25. Joliat, M.J., Umeda, S., Lyons, B.L., Lynes, M.A., and Shultz, L.D. (2002). Establishment and characterization of a new osteogenic cell line (MOS-J) from a spontaneous C57BL=6J mouse oste-osarcoma. In Vivo 16, 223-228.
26. Krause, D.S. (2005). Engraftment of bone marrow-derived epithelial cells. Ann. N. Y. Acad. Sci. 1044, 117-124.
27. Krause, D.S., Theise, N.D., Collector, M.I., Henegariu, O., Hwang, S., Gardner, R., Neutzel, S., and Sharkis, S.J. (2001). Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105, 369-377.
28. Kuang, P.P., Lucey, E., Rishikof, D.C., Humphries, D.E., Brons-nick, D., and Goldstein, R.H. (2005). Engraftment of neonatal lung fibroblasts into the normal and elastase-injured lung. Am. J. Respir. Cell Mol. Biol. 33, 371-377.
29. Lemarchand, P., Jones, M., Danel, C., Yamada, I., Mastrangeli, A., and Crystal, R.G. (1994). In vivo adenovirus-mediated gene transfer to lungs via pulmonary artery. J. Appl. Physiol. 76, 2840-2845. (Pubitemid 24184816)
30. Loebinger, M.R., Aguilar, S., and Janes, S.M. (2008a). Therapeutic potential of stem cells in lung disease: Progress and pitfalls. Clin. Sci. 114, 99-108.
31. Loebinger, M.R., Sage, E.K., and Janes, S.M. (2008b). Mesench-ymal stem cells as vectors for lung disease. Proc. Am. Thorac. Soc. 5, 711-716.
32. 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.
33. MacPherson, H., Keir, P., Webb, S., Samuel, K., Boyle, S., Bick-more, W., Forrester, L., and Dorin, J. (2005). Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo. J. Cell Sci. 118, 2441-2450.
34. MacPherson, H., Keir, P.A., Edwards, C.J., Webb, S., and Dorin, J.R. (2006). Following damage, the majority of bone marrow-derived airway cells express an epithelial marker. Respir. Res. 7, 145.
35. Mall, M.A., Harkema, J.R., Trojanek, J.B., Treis, D., Livraghi, A., Schubert, S., Zhou, Z., Kreda, S.M., Tilley, S.L., Hudson, E.J., O'Neal, W.K., and Boucher, R.C. (2008). Development of chronic bronchitis and emphysema in b-epithelial Na+ channel-overexpressing mice. Am. J. Respir. Crit. Care Med. 177, 730-742.
36. Mastrangeli, A., Danel, C., Rosenfeld, M.A., Stratford-Perricaudet, L., Perricaudet, M., Pavirani, A., Lecocq, J.P., and Crystal, R.G. (1993). Diversity of airway epithelial cell targets for in vivo re-combinant adenovirus-mediated gene transfer. J. Clin. Invest. 91, 225-234.
37. Mei, S.H., McCarter, S.D., Deng, Y., Parker, C.H., Liles, W.C., and Stewart, D.J. (2007). Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med. 4, e269.
38. Murry, C.E., Soonpaa, M.H., Reinecke, H., Nakajima, H., Na-kajima, H.O., Rubart, M., Pasumarthi, K.B., Virag, J.I., Bartel-mez, S.H., Poppa, V., Bradford, G., Dowell, J.D., Williams, D.A., and Field, L.J. (2004). Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428, 664-668.
39. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J.C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 90, 8424-8428.
40. Nikolova, G., Jabs, N., Konstantinova, I., Domogatskaya, A., Tryggvason, K., Sorokin, L., Fassler, R., Gu, G., Gerber, H.P., Ferrara, N., Melton, D.A., and Lammert, E. (2006). The vascular basement membrane: A niche for insulin gene expression and beta cell proliferation. Dev. Cell 10, 397-405.
41. Parsons, D.W., Grubb, B.R., Johnson, L.G., and Boucher, R.C. (1998). Enhanced in vivo airway gene transfer via transient modification of host barrier properties with a surface-active agent. Hum. Gene Ther. 9, 2661-2672.
42. Pereira, R.F., Halford, K.W., O'Hara, M.D., Leeper, D.B., Soko-lov, B.P., Pollard, M.D., Bagasra, O., and Prockop, D.J. (1995). Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc. Natl. Acad. Sci. U.S.A. 92, 4857-4861.
43. Pitard, B., Oudrhiri, N., Lambert, O., Vivien, E., Masson, C., Wetzer, B., Hauchecorne, M., Scherman, D., Rigaud, J.L., Vig-neron, J.P., Lehn, J.M., and Lehn, P. (2001). Sterically stabilized BGTC-based lipoplexes: Structural features and gene transfec-tion into the mouse airways in vivo. J. Gene Med. 3, 478-487.
44. Pringle, I.A., Raman, S., Sharp, W.W., Cheng, S.H., Hyde, S.C., and Gill, D.R. (2005). Detection of plasmid DNA vectors following gene transfer to the murine airways. Gene Ther. 12, 1206-1214.
45. Ricks, D.M., Kutner, R., Zhang, X.Y., Welsh, D.A., and Reiser, J. (2008). Optimized lentiviral transduction of mouse bone marrow-derived mesenchymal stem cells. Stem Cells Dev. 17, 441-450.
46. 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.
47. Robey, T.E., Saiget, M.K., Reinecke, H., and Murry, C.E. (2008). Systems approaches to preventing transplanted cell death in cardiac repair. J. Mol. Cell. Cardiol. 45, 567-581.
48. Sales, V.L., Mettler, B.A., Lopez-Ilasaca, M., Johnson, J.A., Jr., and Mayer, J.E., Jr. (2007). Endothelial progenitor and mes-enchymal stem cell-derived cells persist in tissue-engineered patch in vivo: Application of green and red fluorescent protein-expressing retroviral vector. Tissue Eng. 13, 525-535.
49. Santoni de Sio, F.R., Gritti, A., Cascio, P., Neri, M., Sampaolesi, M., Galli, C., Luban, J., and Naldini, L. (2008). Lentiviral vector gene transfer is limited by the proteasome at postentry steps in various types of stem cells. Stem Cells 26, 2142-2152.
50. Selig, L., Pages, J.C., Tanchou, V., Preveral, S., Berlioz-Torrent, C., Liu, L.X., Erdtmann, L., Darlix, J., Benarous, R., and Be-nichou, S. (1999). Interaction with the p6 domain of the Gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses. J. Virol. 73, 592-600.
51. Serikov, V.B., Popov, B., Mikhailov, V.M., Gupta, N., and Mat-thay, M.A. (2007). Evidence of temporary airway epithelial repopulation and rare clonal formation by BM-derived cells following naphthalene injury in mice. Anat. Rec. 290, 1033-1045.
52. Serrano-Mollar, A., Nacher, M., Gay-Jordi, G., Closa, D., Xaubet, A., and Bulbena, O. (2007). Intratracheal transplantation of alveolar type II cells reverses bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 176, 1261-1268.
53. Southam, D.S., Dolovich, M., O'Byrne, P.M., and Inman, M.D. (2002). Distribution of intranasal instillations in mice: Effects of volume, time, body position, and anesthesia. Am. J. Physiol. Lung Cell Mol. Physiol. 282, L833-L839.
54. Sueblinvong, V., Loi, R., Eisenhauer, P.L., Bernstein, I.M., Suratt, B.T., Spees, J.L., and Weiss, D.J. (2008). Derivation of lung epithelium from human cord blood-derived mesenchymal stem cells. Am. J. Respir. Crit. Care Med. 177, 701-711.
55. Uccelli, A., Moretta, L., and Pistoia, V. (2008). Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8, 726-736.
56. Wagers, A.J., 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.
57. Wang, G., Bunnell, B.A., Painter, R.G., Quiniones, B.C., Tom, S., Lanson, N.A., Jr., Spees, J.L., Bertucci, D., Peister, A., Weiss, D.J., Valentine, V.G., Prockop, D.J., and Kolls, J.K. (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.
58. Weiss, D.J. (2002). Delivery of gene transfer vectors to lung: Obstacles and the role of adjunct techniques for airway administration. Mol. Ther. 6, 148-152.
59. Weiss, D.J., Liggitt, D., and Clark, J.G. (1997). In situ histo-chemical detection of b-galactosidase activity in lung: Assessment of X-Gal reagent in distinguishing lacZ gene expression and endogenous b-galactosidase activity. Hum. Gene Ther. 8, 1545-1554.
60. Wong, A.P., Dutly, A.E., Sacher, A., Lee, H., Hwang, D.M., Liu, M., Keshavjee, S., Hu, J., and Waddell, T.K. (2007). Targeted cell replacement with bone marrow cells for airway epithelial regeneration. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L740-L752.
61. Wong, A.P., Keating, A., Lu, W.Y., Duchesneau, P., Wang, X., Sacher, A., Hu, J., and Waddell, T.K. (2009). Identification of a bone marrow-derived epithelial-like population capable of repopulating injured mouse airway epithelium. J. Clin. Invest. 119, 336-348.
62. Xu, J., Woods, C.R., Mora, A.L., Joodi, R., Brigham, K.L., Iyer, S., and Rojas, M. (2007). Prevention of endotoxin-induced systemic response by bone marrow-derived mesenchymal stem cells in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L131-L141.
63. Xu, J., Qu, J., Cao, L., Sai, Y., Chen, C., He, L., and Yu, L. (2008). Mesenchymal stem cell-based angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. J. Pathol. 214, 472-481.
64. Zufferey, R., Nagy, D., Mandel, R.J., Naldini, L., and Trono, D. (1997). Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15, 871-875