Long-Term Self-Renewal of Postnatal Muscle-derived Stem Cells

Molecular Biology of the Cell - Tập 16 Số 7 - Trang 3323-3333 - 2005
Bridget M. Deasy1,2,3, Burhan Gharaibeh3, Jonathan B. Pollett3, Marion Jones3, Michael Lucas3, Yasunari Kanda3, Johnny Huard4,5,2,3
1Department of Bioengineering, Children's Hospital of Pittsburgh, Pittsburgh, PA 15213, USA.
2Departments of Orthopaedic Surgery, University of Pittsburgh, Pittsburgh, PA 15260
3Growth and Development Laboratory, Children's Hospital of Pittsburgh, Pittsburgh, PA 15213.
4Department of Bioengineering, Children's Hospital of Pittsburgh, Pittsburgh, PA 15213
5Departments of Molecular Genetics and Biochemistry, University of Pittsburgh, Pittsburgh, PA 15260

Tóm tắt

The ability to undergo self-renewal is a defining characteristic of stem cells. Self-replenishing activity sustains tissue homeostasis and regeneration. In addition, stem cell therapy strategies require a heightened understanding of the basis of the self-renewal process to enable researchers and clinicians to obtain sufficient numbers of undifferentiated stem cells for cell and gene therapy. Here, we used postnatal muscle-derived stem cells to test the basic biological assumption of unlimited stem cell replication. Muscle-derived stem cells (MDSCs) expanded for 300 population doublings (PDs) showed no indication of replicative senescence. MDSCs preserved their phenotype (ScaI+/CD34+/desminlow) for 200 PDs and were capable of serial transplantation into the skeletal muscle of mdx mice, which model Duchenne muscular dystrophy. MDSCs expanded to this level exhibited high skeletal muscle regeneration comparable with that exhibited by minimally expanded cells. Expansion beyond 200 PDs resulted in lower muscle regeneration, loss of CD34 expression, loss of myogenic activity, and increased growth on soft agar, suggestive of inevitable cell aging attributable to expansion and possible transformation of the MDSCs. Although these results raise questions as to whether cellular transformations derive from cell culturing or provide evidence of cancer stem cells, they establish the remarkable long-term self-renewal and regeneration capacity of postnatal MDSCs.

Từ khóa


Tài liệu tham khảo

Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J., and Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells.Proc. Natl. Acad. Sci. USA100, 3983–3988.

Amit, M., Carpenter, M. K., Inokuma, M. S., Chiu, C. P., Harris, C. P., Waknitz, M. A., Itskovitz-Eldor, J., and Thomson, J. A. (2000). Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture.Dev. Biol.227, 271–278.

Berghella, L.et al. (1999). Reversible immortalization of human myogenic cells by site-specific excision of a retrovirally transferred oncogene.Hum. Gene Ther.10, 1607–1617.

Bhardwaj, G., Murdoch, B., Wu, D., Baker, D. P., Williams, K. P., Chadwick, K., Ling, L. E., Karanu, F. N., and Bhatia, M. (2001). Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation.Nat. Immunol.2, 172–180.

Bianchi, G., Banfi, A., Mastrogiacomo, M., Notaro, R., Luzzatto, L., Cancedda, R., and Quarto, R. (2003). Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2.Exp. Cell Res.287, 98–105.

Bonnet, D., and Dick, J. E. (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell.Nat. Med.3, 730–737.

Cobaleda, C., Gutierrez-Cianca, N., Perez-Losada, J., Flores, T., Garcia-Sanz, R., Gonzalez, M., and Sanchez-Garcia, I. (2000). A primitive hematopoietic cell is the target for the leukemic transformation in human Philadelphia-positive acute lymphoblastic leukemia.Blood95, 1007–1013.

Colter, D. C., Class, R., DiGirolamo, C. M., and Prockop, D. J. (2000). Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow.Proc. Natl. Acad. Sci. USA97, 3213–3218.

Deasy, B. M., and Huard, J. (2002). Gene therapy and tissue engineering based on muscle-derived stem cells.Curr. Opin. Mol. Ther.4, 382–389.

Deasy, B. M., Jankowski, R. J., Payne, T. R., Cao, B., Goff, J. P., Greenberger, J. S., and Huard, J. (2003). Modeling stem cell population growth: incorporating terms for proliferative heterogeneity.Stem Cells21, 536–545.

Dick, J. E. (2003). Breast cancer stem cells revealed.Proc. Natl. Acad. Sci. USA100, 3547–3549.

Digirolamo, C. M., Stokes, D., Colter, D., Phinney, D. G., Class, R., and Prockop, D. J. (1999). Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate.Br. J. Haematol.107, 275–281.

Gilmore, G. L., DePasquale, D. K., Lister, J., and Shadduck, R. K. (2000). Ex vivo expansion of human umbilical cord blood and peripheral blood CD34(+) hematopoietic stem cells.Exp. Hematol.28, 1297–1305.

Hayflick, L., and Moorhead, P. S. (1961). The serial cultivation of human diploid cell strains.Exp. Cell Res.25, 585–621.

Hemmati, H. D., Nakano, I., Lazareff, J. A., Masterman-Smith, M., Geschwind, D. H., Bronner-Fraser, M., and Kornblum, H. I. (2003). Cancerous stem cells can arise from pediatric brain tumors.Proc. Natl. Acad. Sci. USA100, 15178–15183.

Irintchev, A., Zeschnigk, M., Starzinski-Powitz, A., and Wernig, A. (1994). Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles.Dev. Dyn.199, 326–337.

Jankowski, R. J., Deasy, B. M., Cao, B., Gates, C., and Huard, J. (2002). The role of CD34 expression and cellular fusion in the regeneration capacity of myogenic progenitor cells.J. Cell Sci.115, 4361–4374.

Jiang, Y., Henderson, D., Blackstad, M., Chen, A., Miller, R. F., and Verfaillie, C. M. (2003). Neuroectodermal differentiation from mouse multipotent adult progenitor cells.Proc. Natl. Acad. Sci. USA100(suppl 1), 11854–11860.

Jiang, Y.et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow.Nature418, 41–49.

Karanu, F. N., Murdoch, B., Gallacher, L., Wu, D. M., Koremoto, M., Sakano, S., and Bhatia, M. (2000). The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells.J. Exp. Med.192, 1365–1372.

Knobel, K. M., McNally, M. A., Berson, A. E., Rood, D., Chen, K., Kilinski, L., Tran, K., Okarma, T. B., and Lebkowski, J. S. (1994). Long-term reconstitution of mice after ex vivo expansion of bone marrow cells: differential activity of cultured bone marrow and enriched stem cell populations.Exp. Hematol.22, 1227–1235.

Knudson, A. G. (2001). Two genetic hits (more or less) to cancer.Nat. Rev. Cancer1, 157–162.

Lee, J. Y.et al. (2000). Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing.J. Cell Biol.150, 1085–1100.

Miyamoto, T., Weissman, I. L., and Akashi, K. (2000). AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation.Proc. Natl. Acad. Sci. USA97, 7521–7526.

Molofsky, A. V., Pardal, R., and Morrison, S. J. (2004). Diverse mechanisms regulate stem cell self-renewal.Curr. Opin. Cell Biol.16, 700–707.

Muraglia, A., Cancedda, R., and Quarto, R. (2000). Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model.J. Cell Sci.113, 1161–1166.

Peters, S. O., Kittler, E. L., Ramshaw, H. S., and Quesenberry, P. J. (1995). Murine marrow cells expanded in culture with IL-3, IL-6, IL-11, and SCF acquire an engraftment defect in normal hosts.Exp. Hematol.23, 461–469.

Piacibello, W., Sanavio, F., Garetto, L., Severino, A., Bergandi, D., Ferrario, J., Fagioli, F., Berger, M., and Aglietta, M. (1997). Extensive amplification and self-renewal of human primitive hematopoietic stem cells from cord blood.Blood89, 2644–2653.

Potten, C. S., and Morris, R. J. (1988). Epithelial stem cells in vivo.J. Cell Sci.(suppl)10, 45–62.

Qu-Petersen,et al. (2002). Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration.J. Cell Biol.157, 851–864.

Reya, T., Morrison, S. J., Clarke, M. F., and Weissman, I. L. (2001). Stem cells, cancer, and cancer stem cells.Nature414, 105–111.

Reyes, M., Lund, T., Lenvik, T., Aguiar, D., Koodie, L., and Verfaillie, C. M. (2001). Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells.Blood98, 2615–2625.

Rombouts, W. J., and Ploemacher, R. E. (2003). Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture.Leukemia17, 160–170.

Rubin, H. (1997). Cell aging in vivo and in vitro.Mech. Ageing Dev.98, 1–35.

Rubin, H. (2002). The disparity between human cell senescence in vitro and lifelong replication in vivo.Nat. Biotechnol.20, 675–681.

Seale, P., Asakura, A., and Rudnicki, M. A. (2001). The potential of muscle stem cells.Dev. Cell.1, 333–342.

Seale, P., Sabourin, L. A., Girgis-Gabardo, A., Mansouri, A., Gruss, P., and Rudnicki, M. A. (2000). Pax7 is required for the specification of myogenic satellite cells.Cell102, 777–786.

Sherley, J. L., Stadler, P. B., and Stadler, J. S. (1995). A quantitative method for the analysis of mammalian cell proliferation in culture in terms of dividing and non-dividing cells.Cell Prolif.28, 137–144.

Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., and Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors.Cancer Res.63, 5821–5828.

Smith, A. G. (2001). Embryo-derived stem cells: of mice and men.Annu. Rev. Cell. Dev. Biol.17, 435–462.

Stiles, B., Groszer, M., Wang, S., Jiao, J., and Wu, H. (2004). PTENless means more.Dev. Biol.273, 175–184.

Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts.Science282, 1145–1147.

Traycoff, C. M., Cornetta, K., Yoder, M. C., Davidson, A., and Srour, E. F. (1996). Ex vivo expansion of murine hematopoietic progenitor cells generates classes of expanded cells possessing different levels of bone marrow repopulating potential.Exp. Hematol.24, 299–306.

van Noort, M., and Clevers, H. (2002). TCF transcription factors, mediators of Wnt-signaling in development and cancer.Dev. Biol.244, 1–8.

Varnum-Finney, B., Xu, L., Brashem-Stein, C., Nourigat, C., Flowers, D., Bakkour, S., Pear, W. S., and Bernstein, I. D. (2000). Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling.Nat. Med.6, 1278–1281.

Xu, C., Inokuma, M. S., Denham, J., Golds, K., Kundu, P., Gold, J. D., and Carpenter, M. K. (2001). Feeder-free growth of undifferentiated human embryonic stem cells.Nat. Biotechnol.19, 971–974.

Zammit, P., and Beauchamp, J. (2001). The skeletal muscle satellite cell: stem cell or son of stem cell?Differentiation68, 193–204.

Zipori, D. (2004). The nature of stem cells: state rather than entity.Nat. Rev. Genet.5, 873–878.

Thông tin
Thông tin xuất bản

Molecular Biology of the Cell

Tập 16 Số 7

3323-3333

Thông tin tác giả