{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,6]],"date-time":"2026-02-06T06:35:01Z","timestamp":1770359701036,"version":"3.49.0"},"reference-count":36,"publisher":"The Company of Biologists","issue":"11","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2005,6,1]]},"abstract":"<jats:p>Recent work has indicated that adult bone marrow-derived cells have the ability to contribute to both the haematopoietic system and other organs. Haematopoietic reconstitution by whole bone marrow and selected but not fully characterised cell populations have resulted in reports indicating high-level repopulation of lung epithelia. The well-characterised cells from the side population have a robust ability for haematopoietic reconstitution. We have used freshly isolated side population cells derived from ROSA26 adult bone marrow and demonstrate that despite being unable to contribute to embryos following blastocyst injection, or air liquid interface cultures or denuded tracheal xenografts, they could contribute to the tracheal epithelium in vivo. Epithelial damage is reported to be important in encouraging the recruitment of marrow-derived stem cells into non-haematopoietic organs. Here we demonstrate that mice engrafted with side population cells have donor-derived cells present in the epithelial lining of the trachea following damage and repair. Donor-derived cells were found at a frequency of 0.83%. Widefield and confocal microscopy revealed donor cells that expressed cytokeratins, indicative of cells of an epithelial nature. These results imply that SP haematopoietic stem cells from the bone marrow do not have the ability to contribute to airway epithelia themselves but require factors present in vivo to allow them to acquire characteristics of this tissue.<\/jats:p>","DOI":"10.1242\/jcs.02375","type":"journal-article","created":{"date-parts":[[2005,5,28]],"date-time":"2005-05-28T21:13:14Z","timestamp":1117314794000},"page":"2441-2450","source":"Crossref","is-referenced-by-count":67,"title":["Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo"],"prefix":"10.1242","volume":"118","author":[{"given":"Heather","family":"MacPherson","sequence":"first","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pamela","family":"Keir","sequence":"additional","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sheila","family":"Webb","sequence":"additional","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kay","family":"Samuel","sequence":"additional","affiliation":[{"name":"Scottish National Blood Transfusion Service, John Hughes Bennett Laboratory, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shelagh","family":"Boyle","sequence":"additional","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wendy","family":"Bickmore","sequence":"additional","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lesley","family":"Forrester","sequence":"additional","affiliation":[{"name":"John Hughes Bennett Laboratory, University of Edinburgh, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julia","family":"Dorin","sequence":"additional","affiliation":[{"name":"MRC Human Genetics Unit, Western General Hospital, Crewe Road South, Edinburgh, EH4 2XU, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","reference":[{"key":"2021042518491708400_REF1","doi-asserted-by":"crossref","unstructured":"Alvarez-Dolado, M., Pardal, R., Garcia-Verdugo, J. M., Fike, J. R., Lee, H. O., Pfeffer, K., Lois, C., Morrison, S. J. and Alvarez-Buylla, A. (2003). Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature425, 968-973.","DOI":"10.1038\/nature02069"},{"key":"2021042518491708400_REF2","doi-asserted-by":"crossref","unstructured":"Asakura, A., Seale, P., Girgis-Gabardo, A. and Rudnicki, M. A. (2002). Myogenic specification of side population cells in skeletal muscle. J. Cell Biol.159, 123-134.","DOI":"10.1083\/jcb.200202092"},{"key":"2021042518491708400_REF3","doi-asserted-by":"crossref","unstructured":"Balsam, L. B., Wagers, A. J., Christensen, J. L., Kofidis, T., Weissman, I. L. and Robbins, R. C. (2004). Haematopoietic stem cells adopt mature haematopoietic fates in ischaemic myocardium. Nature428, 668-673.","DOI":"10.1038\/nature02460"},{"key":"2021042518491708400_REF4","doi-asserted-by":"crossref","unstructured":"Borthwick, D. W., West, J. D., Keighren, M. A., Flockhart, J. H., Innes, B. A. and Dorin, J. R. (1999). Murine submucosal glands are clonally derived and show a cystic fibrosis gene-dependent distribution pattern. Am. J. Respir. Cell Mol. Biol.20, 1181-1189.","DOI":"10.1165\/ajrcmb.20.6.3475"},{"key":"2021042518491708400_REF5","doi-asserted-by":"crossref","unstructured":"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.","DOI":"10.1165\/ajrcmb.24.6.4217"},{"key":"2021042518491708400_REF6","doi-asserted-by":"crossref","unstructured":"Brittan, M., Braun, K. M., Reynolds, L. E., Conti, F. J., Reynolds, A. R., Poulsom, R., Alison, M. R., Wright, N. A. and Hodivala-Dilke, K. M. (2005). Bone marrow cells engraft within the epidermis and proliferate in vivo with no evidence of cell fusion. J. Pathol.205, 1-13.","DOI":"10.1002\/path.1682"},{"key":"2021042518491708400_REF7","doi-asserted-by":"crossref","unstructured":"Camargo, F. D., Green, R., Capetenaki, Y., Jackson, K. A. and Goodell, M. A. (2003). Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat. Med.9, 1520-1527.","DOI":"10.1038\/nm963"},{"key":"2021042518491708400_REF8","doi-asserted-by":"crossref","unstructured":"Camargo, F. D., Finegold, M. and Goodell, M. A. (2004). Hematopoietic myelomonocytic cells are the major source of hepatocyte fusion partners. J. Clin. Invest113, 1266-1270.","DOI":"10.1172\/JCI21301"},{"key":"2021042518491708400_REF9","doi-asserted-by":"crossref","unstructured":"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. Science297, 1299.","DOI":"10.1126\/science.297.5585.1299"},{"key":"2021042518491708400_REF10","doi-asserted-by":"crossref","unstructured":"Clarke, D. L., Johansson, C. B., Wilbertz, J., Veress, B., Nilsson, E., Karlstrom, H., Lendahl, U. and Frisen, J. (2000). Generalized potential of adult neural stem cells. Science288, 1660-1663.","DOI":"10.1126\/science.288.5471.1660"},{"key":"2021042518491708400_REF11","doi-asserted-by":"crossref","unstructured":"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.","DOI":"10.1165\/rcmb.2004-0079RC"},{"key":"2021042518491708400_REF12","doi-asserted-by":"crossref","unstructured":"Davidson, D. J., Kilanowski, F. M., Randell, S. H., Sheppard, D. N. and Dorin, J. R. (2000). A primary culture model of differentiated murine tracheal epithelium. Am. J. Physiol Lung Cell Mol. Physiol279, L766-L778.","DOI":"10.1152\/ajplung.2000.279.4.L766"},{"key":"2021042518491708400_REF13","doi-asserted-by":"crossref","unstructured":"Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G. and Mavilio, F. (1998). 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Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med.3, 1337-1345.","DOI":"10.1038\/nm1297-1337"},{"key":"2021042518491708400_REF17","doi-asserted-by":"crossref","unstructured":"Grove, J. E., Lutzko, C., Priller, J., Henegariu, O., Theise, N. D., Kohn, D. B. and Krause, D. S. (2002). Marrow-derived cells as vehicles for delivery of gene therapy to pulmonary epithelium. Am. J. Respir. Cell Mol. Biol.27, 645-651.","DOI":"10.1165\/rcmb.2002-0056RC"},{"key":"2021042518491708400_REF18","doi-asserted-by":"crossref","unstructured":"Gussoni, E., Soneoka, Y., Strickland, C. D., Buzney, E. A., Khan, M. K., Flint, A. F., Kunkel, L. M. and Mulligan, R. C. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature401, 390-394.","DOI":"10.1038\/43919"},{"key":"2021042518491708400_REF19","doi-asserted-by":"crossref","unstructured":"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. Science305, 90-93.","DOI":"10.1126\/science.1098925"},{"key":"2021042518491708400_REF20","doi-asserted-by":"crossref","unstructured":"Jackson, K. A., Majka, S. M., Wang, H., Pocius, J., Hartley, C. J., Majesky, M. W., Entman, M. L., Michael, L. H., Hirschi, K. K. and Goodell, M. A. (2001). Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J. Clin. Invest107, 1395-1402.","DOI":"10.1172\/JCI12150"},{"key":"2021042518491708400_REF21","doi-asserted-by":"crossref","unstructured":"Jiang, Y., Jahagirdar, B. N., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M. et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature418, 41-49.","DOI":"10.1038\/nature00870"},{"key":"2021042518491708400_REF22","doi-asserted-by":"crossref","unstructured":"Korbling, M., Katz, R. L., Khanna, A., Ruifrok, A. C., Rondon, G., Albitar, M., Champlin, R. E. and Estrov, Z. (2002). Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. New Engl. J. Med.346, 738-746.","DOI":"10.1056\/NEJMoa3461002"},{"key":"2021042518491708400_REF23","doi-asserted-by":"crossref","unstructured":"Kotton, D. N., Ma, B. Y., Cardoso, W. V., Sanderson, E. A., Summer, R. S., Williams, M. C. and Fine, A. (2001). Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development128, 5181-5188.","DOI":"10.1242\/dev.128.24.5181"},{"key":"2021042518491708400_REF24","doi-asserted-by":"crossref","unstructured":"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. Cell105, 369-377.","DOI":"10.1016\/S0092-8674(01)00328-2"},{"key":"2021042518491708400_REF25","doi-asserted-by":"crossref","unstructured":"LaBarge, M. A. and Blau, H. M. (2002). Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell111, 589-601.","DOI":"10.1016\/S0092-8674(02)01078-4"},{"key":"2021042518491708400_REF26","doi-asserted-by":"crossref","unstructured":"Lagasse, E., Connors, H., Al Dhalimy, M., Reitsma, M., Dohse, M., Osborne, L., Wang, X., Finegold, M., Weissman, I. L. and Grompe, M. (2000). Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med.6, 1229-1234.","DOI":"10.1038\/81326"},{"key":"2021042518491708400_REF27","doi-asserted-by":"crossref","unstructured":"Lapidos, K. A., Chen, Y. E., Earley, J. U., Heydemann, A., Huber, J. M., Chien, M., Ma, A. and McNally, E. M. (2004). Transplanted hematopoietic stem cells demonstrate impaired sarcoglycan expression after engraftment into cardiac and skeletal muscle. J. Clin. Invest114, 1577-1585.","DOI":"10.1172\/JCI200423071"},{"key":"2021042518491708400_REF28","doi-asserted-by":"crossref","unstructured":"Mezey, E., Chandross, K. J., Harta, G., Maki, R. A. and McKercher, S. R. (2000). Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science290, 1779-1782.","DOI":"10.1126\/science.290.5497.1779"},{"key":"2021042518491708400_REF29","doi-asserted-by":"crossref","unstructured":"Murry, C. E., Soonpaa, M. H., Reinecke, H., Nakajima, H., Nakajima, H. O., Rubart, M., Pasumarthi, K. B., Virag, J. I., Bartelmez, S. H., Poppa, V. et al. (2004). Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature428, 664-668.","DOI":"10.1038\/nature02446"},{"key":"2021042518491708400_REF30","doi-asserted-by":"crossref","unstructured":"Newsome, P. N., Johannessen, I., Boyle, S., Dalakas, E., McAulay, K. A., Samuel, K., Rae, F., Forrester, L., Turner, M. L., Hayes, P. C. et al. (2003). Human cord blood-derived cells can differentiate into hepatocytes in the mouse liver with no evidence of cellular fusion. Gastroenterology124, 1891-1900.","DOI":"10.1016\/S0016-5085(03)00401-3"},{"key":"2021042518491708400_REF31","doi-asserted-by":"crossref","unstructured":"Okamoto, R., Yajima, T., Yamazaki, M., Kanai, T., Mukai, M., Okamoto, S., Ikeda, Y., Hibi, T., Inazawa, J. and Watanabe, M. (2002). Damaged epithelia regenerated by bone marrow#150;derived cells in the human gastrointestinal tract. Nat. Med.8, 1011-1017.","DOI":"10.1038\/nm755"},{"key":"2021042518491708400_REF32","doi-asserted-by":"crossref","unstructured":"Olmsted-Davis, E. A., Gugala, Z., Camargo, F., Gannon, F. H., Jackson, K., Kienstra, K. A., Shine, H. D., Lindsey, R. W., Hirschi, K. K., Goodell, M. A. et al. (2003). Primitive adult hematopoietic stem cells can function as osteoblast precursors. Proc. Natl. Acad. Sci. USA100, 15877-15882.","DOI":"10.1073\/pnas.2632959100"},{"key":"2021042518491708400_REF33","doi-asserted-by":"crossref","unstructured":"Theise, N. D., Henegariu, O., Grove, J., Jagirdar, J., Kao, P. N., Crawford, J. M., Badve, S., Saxena, R. and Krause, D. S. (2002). Radiation pneumonitis in mice: a severe injury model for pneumocyte engraftment from bone marrow. Exp. Hematol.30, 1333-1338.","DOI":"10.1016\/S0301-472X(02)00931-1"},{"key":"2021042518491708400_REF34","doi-asserted-by":"crossref","unstructured":"Wagers, A. J. and Weissman, I. L. (2004). Plasticity of adult stem cells. Cell116, 639-648.","DOI":"10.1016\/S0092-8674(04)00208-9"},{"key":"2021042518491708400_REF35","doi-asserted-by":"crossref","unstructured":"Wagers, A. J., Sherwood, R. I., Christensen, J. L. and Weissman, I. L. (2002). Little evidence for developmental plasticity of adult hematopoietic stem cells. 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