Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential

Journal of Cell Science

Volumn 117, Issue 14, 2004, Pages 2971-2981

  D'Ippolito, Gianluca ^a   Diabira, Sylma ^a,b,c   Howard, Guy A ^a   Menei, Philippe ^b,c   Roos, Bernard A ^a   Schiller, Paul C ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ D'ANGERS   (France)

^c INSERM   (France)

Author keywords

Aging; Bone marrow; Neurogenesis; Pluripotential; Reparative medicine; Stem cells

Indexed keywords

BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; CD34 ANTIGEN; CD36 ANTIGEN; CD45 ANTIGEN; CD63 ANTIGEN; CD81 ANTIGEN; FIBRONECTIN; HLA DR ANTIGEN; INTERLEUKIN 2 RECEPTOR BETA; REX PROTEIN; SCATTER FACTOR RECEPTOR; STEM CELL FACTOR RECEPTOR; TELOMERASE; TYROSINE KINASE RECEPTOR;

ADIPOCYTE; ADOLESCENT; ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW CELL; CARTILAGE CELL; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL POPULATION; CELL SELECTION; CHILD; CONTROLLED STUDY; ECTODERM; ENDODERM; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MESODERM; MICROENVIRONMENT; NERVE CELL; NUCLEOTIDE SEQUENCE; OSTEOBLAST; OXYGEN TENSION; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE;

ADIPOCYTES; ADOLESCENT; ADULT; AGED; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; CHONDROCYTES; ECTODERM; ENDODERM; FEMALE; HUMANS; ISLETS OF LANGERHANS; MALE; MESODERM; MIDDLE AGED; NEURONS; OSTEOBLASTS; STEM CELLS;

BOVINAE;

EID: 4344645792     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01103     Document Type: Article

References (51)

1. Asahara, T., Takahashi, T., Masuda, H., Kalka, C., Chen, D., Iwaguro, H., Inai, Y., Silver, M. and Isner, J. M. (1999). VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 18, 3964-3972.
2. Asakura, A. and Rudnicki, M. A. (2002). Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp. Hematol. 30, 1339-1345.
3. Brazelton, T. R., Rossi, F. M., Keshet, G. I. and Blau, H. M. (2000). Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Science 290, 1775-1779.
4. Chow, D. C., Wenning, L. A., Miller, W. M. and Papoutsakis, E. T. (2001). Modeling pO(2) distributions in the bone marrow hematopoietic compartment. I. Krogh's model. Biophys. J. 81, 675-684.
5. Cipolleschi, M. G., Dello-Sbarba, P. and Olivotto, M. (1993). The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 82, 2031-2037.
6. 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. USA 97, 3213-3218.
7. Colter, D. C., Sekiya, I. and Prockop, D. J. (2001). Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal-cells. Proc. Natl. Acad. Sci. USA 98, 7841-7845.
8. Conget, P. A. and Minguell, J. J. (1999). Phenotypical and functional properties of human bone marrow mesenchymal progenitor cells. J. Cell. Physiol. 181, 67-73.
9. med,low phenotype. Br. J. Haematol. 122, 506-517.
10. D'Ippolito, G., Schiller, P. C., Roos, B. A., Ricordi, C. and Howard, G. A. (1999). Age related changes in the osteogenic potential of human mesenchymal stem cells. J. Bone Miner Res. 14, 1115-1122.
11. 3 in osteoblastic differentiation of human vertebral bone marrow stromal cells. Bone 31, 269-275.
12. 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.
13. Erices, A., Conget, P. and Minguell, J. J. (2000). Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 109, 235-242.
14. Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G. and Mavilio, F. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528-1530.
15. Friedenstein, A. J., Chailakhjan, R. K. and Lalykina, K. S. (1970). The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 3, 393-403.
16. Gronthos, S., Zannettino, A. C., Hay, S. J., Shi, S., Graves, S. E., Kortesidis, A. and Simmons, P. J. (2003). Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J. Cell Sci. 116, 1827-1835.
17. Hayflick, L. and Moorhead, P. S. (1961). The serial cultivation of human diploid cell strains. Exp. Cell. Res. 25, 585-621.
18. Hung, S. C., Chen, N. J., Hsieh, S. L., Li, H., Ma, H. L. and Lo, W. H. (2002). Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 20, 249-258.
19. Hunziker, E. and Stein, M. (2000). Nestin-expressing cells in the pancreatic islets of Langerhans. Biochem. Biophys. Res. Commun. 271, 116-119.
20. Huss, R. (2000). Isolation of primary and immortalized CD34-hematopoietic and mesenchymal stem cells from various sources. Stem Cells 18, 1-9.
21. 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. Nature 418, 41-49.
22. Kopen, G. C., Prockop, D. J. and Phinney, D. G. (1999). Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. USA 96, 10711-10716.
23. Krause, D. S., Theise, N. D., Collector, M. L, 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.
24. - stem cells that give rise to SCID-repopulating cells. Blood 101, 869-876.
25. Lord, B. I. (1992). The architecture of bone marrow cell populations. In Concise Reviews in Clinical and Experimental Haematology (ed. M. Murphy Jr), Dayton, OH, USA: AlphaMed Press.
26. Lumelsky, N., Blondel, O., Laeng, P., Velasco, I., Ravin, R. and McKay, R. (2001). Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292, 1389-1394.
27. Mackay, A. M., Beck, S. C., Murphy, J. M., Barry, F. P., Chichester, C. O. and Pittenger, M. F. (1998). Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue. Eng. 4, 415-428.
28. McCarthy, M., Auger, D. and Whittemore, S. R. (2000). Human cytomegalovirus causes productive infection and neuronal injury in differentiating fetal human central nervous system neuroepithelial precursor cells. J Hum. Virol. 3, 215-228.
29. Mezey, E., Key, S., Vogelsang, G., Szalayova, L, Lange, G. D. and Crain, B. (2003). Transplanted bone marrow generates new neurons in human brains. Proc. Natl. Acad. Sci. USA 100, 1364-1369.
30. Movassat, J., Beattie, G. M., Lopez, A. D. and Hayek, A. (2002). Exendin 4 up-regulates expression of PDX 1 and hastens differentiation and maturation of human fetal pancreatic cells. J. Clin. Endocrinol. Metab. 87, 4775-4781.
31. Orlic, D., Kajstura, J., Chimenti, S., Limana, E., Jakoniuk, L, Quaini, F., Nadal-Ginard, B., Bodine, D. M., Leri, A. and Anversa, P. (2001). Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc. Natl. Acad. Sci. USA 98, 10344-10349.
32. Pittenger, M. F., Mackai, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S. and Marshak, D. R. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147.
33. 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. Blood 98, 2615-2625.
34. Schiller, P. C., D'Ippolito, G., Balkan, W., Roos, B. A. and Howard, G. A. (2001a). Gap-junctional communication mediates parathyroid hormone stimulation of mineralization in osteoblastic cultures. Bone 28, 38-44.
35. Schiller, P. C., D'Ippolito, G., Balkan, W., Roos, B. A. and Howard, G. A. (2001b). Gap-junctional communication is required for the maturation process of osteoblastic cells in culture. Bone 28, 362-369.
36. Schiller, P. C., D'Ippolito, G., Brambilla, R., Roos, B. A. and Howard, G. A. (2001c). Inhibition of gap-junctional communication induces the trans-differentiation of osteoblasts to an adipocytic phenotype in vitro. J. Biol. Chem. 276, 14133-14138.
37. Schwartz, R. E., Reyes, M., Koodie, L., Jiang, Y., Blackstad, M., Lund, T., Lenvik, T., Johnson, S., Hu, W. S. and Verfaillie, C. M. (2002). Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J. Clin. Invest. 109, 1291-1302.
38. Soria, B. (2001). In-vitro differentiation of pancreatic beta-cells. Differentiation 68, 205-219.
39. Terada, N., Hamazaki, T., Oka, M., Hoki, M., Mastalerz, D. M., Nakano, Y., Meyer, E. M., Morel, L., Petersen, B. E. and Scott, E. W. (2002). Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416, 542-545.
40. Theise, N. D., Badve, S., Saxena, R., Henegariu, O., Sell, S., Crawford, J. M. and Krause, D. S. (2000). Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31, 235-240.
41. Toma, J. G., Akhavan, M., Fernandes, K. J. L., Bernabé-Heider, F., Sadikos, A., Kaplan, D. R. and Miller, F. D. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biol. 3, 778-784.
42. Tremain, N., Korkko, J., Ibberson, D., Kopen, G. C., DiGirolamo, C. and Phinney, D. G. (2001). MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 19, 408-418.
43. Watt, E. M. and Hogan, B. L. (2000). Out of Eden: stem cells and their niches. Science 287, 1427-1430.
44. Ying, Q. L., Nichols, J., Evans, E. P. and Smith, A. G. (2002). Changing potency by spontaneous fusion. Nature 416, 545-548.
45. Young, H. E., Steele, T. A., Bray, R. A., Detmer, K., Blake, L. W., Lucas, P. W. and Black, A. C. Jr (1999). Human pluripotent and progenitor cells display cell surface cluster differentiation markers CD10, CD13, CD56, and MHC class-I. Proc. Soc. Exp. Biol. Med. 221, 63-71.
46. Young, H. E., Steele, T. A., Bray, R. A., Hudson, J., Floyd, J. A., Hawkins, K., Thomas, K., Austin, T., Edwards, C., Cuzzourt, J. et al. (2001). Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat. Rec. 264, 51-62.
47. Young, R. G., Butler, D. L., Weber, W., Caplan, A. L, Gordon, S. L. and Fink, D. J. (1998). Use of mesenchymal stem cells in a collagen matrix for Achilles tendon repair. J. Orthop. Res. 16, 406-413.
48. Zhao, L. R., Duan, W. M., Reyes, M., Keene, C. D., Verfaillie, C. M. and Low, W. C. (2002). Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp. Neurol. 174, 11-20.
49. Zuk, P. A., Zhu, M., Mizuno, H., Huang, J., Futrell, J. W., Katz, A. J., Benhaim, P., Lorenz, H. P. and Hedrick, M. H. (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211-228.
50. Zulewski, H., Abraham, E. J., Gerlach, M. J., Daniel, P. B., Moritz, W., Muller, B., Vallejo, M., Thomas, M. K. and Habener, J. F. (2001). Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes 50, 521-533.
51. Zvaifler, N. J., Marinova-Mutafchieva, L., Adams, G., Edwards, C. J., Moss, J. and Burger, J. A. and Maini, R. N. (2000). Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res. 2, 477-498.