Can bone marrow-derived stem cells differentiate into functional neurons?

Experimental Neurology

Volumn 193, Issue 2, 2005, Pages 273-278

  Lu, P ^a   Tuszynski, M H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; CYTOFLUOROMETRY; GENE EXPRESSION; GLIA CELL; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE SPECIFICITY;

EID: 18144428744     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2005.01.031     Document Type: Note

References (66)

1. A. Abouelfetouh, T. Kondoh, K. Ehara, and E. Kohmura Morphological differentiation of bone marrow stromal cells into neuron-like cells after co-culture with hippocampal slice Brain Res. 1029 2004 114 119
2. M. Alvarez-Dolado, R. Pardal, J.M. Garcia-Verdugo, J.R. Fike, H.O. Lee, K. Pfeffer, C. Lois, S.J. Morrison, and A. Alvarez-Buylla Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes Nature 425 2003 968 973
3. S. Bonilla, P. Alarcon, R. Villaverde, P. Aparicio, A. Silva, and S. Martinez Haematopoietic progenitor cells from adult bone marrow differentiate into cells that express oligodendroglial antigens in the neonatal mouse brain Eur. J. Neurosci. 15 2002 575 582
4. P. Bossolasco, L. Cova, C. Calzarossa, S.G. Rimoldi, C. Borsotti, G. Lambertenghi Deliliers, V. Silani, and D. Soligo Neuro-glial differentiation of human bone marrow stem cells in vitro Exp. Neurol. 2005 doi:10.1016/j.expneurol. 2004.12.013
5. T.R. Brazelton, F.M. Rossi, G.I. Keshet, and H.M. Blau From marrow to brain: expression of neuronal phenotypes in adult mice Science 290 2000 1775 1779
6. R.F. Castro, K.A. Jackson, M.A. Goodell, C.S. Robertson, H. Liu, and H.D. Shine Failure of bone marrow cells to transdifferentiate into neural cells in vivo Science 297 2002 1299
7. S. Corti, F. Locatelli, C. Donadoni, S. Strazzer, S. Salani, R. Del Bo, M. Caccialanza, N. Bresolin, G. Scarlato, and G.P. Comi Neuroectodermal and microglial differentiation of bone marrow cells in the mouse spinal cord and sensory ganglia J. Neurosci. Res. 70 2002 721 733
8. W. Deng, M. Obrocka, I. Fischer, and D.J. Prockop In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP Biochem. Biophys. Res. Commun. 282 2001 148 152
9. M. Dezawa, H. Kanno, M. Hoshino, H. Cho, N. Matsumoto, Y. Itokazu, N. Tajima, H. Yamada, H. Sawada, H. Ishikawa, T. Mimura, M. Kitada, Y. Suzuki, and C. Ide Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation J. Clin. Invest. 113 2004 1701 1710
10. J. Goolsby, M.C. Marty, D. Heletz, J. Chiappelli, G. Tashko, D. Yarnell, P.S. Fishman, S. Dhib-Jalbut, C.T. Bever Jr., B. Pessac, and D. Trisler Hematopoietic progenitors express neural genes Proc. Natl. Acad. Sci. U. S. A. 100 2003 14926 14931
11. J.E. Grove, E. Bruscia, and D.S. Krause Plasticity of bone marrow-derived stem cells Stem Cells 22 2004 487 500
12. A. Hermann, R. Gastl, S. Liebau, M.O. Popa, J. Fiedler, B.O. Boehm, M. Maisel, H. Lerche, J. Schwarz, R. Brenner, and A. Storch Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells J. Cell. Sci. 117 2004 4411 4422
13. D.C. Hess, T. Abe, W.D. Hill, A.M. Studdard, J. Carothers, M. Masuya, P.A. Fleming, C.J. Drake, and M. Ogawa Hematopoietic origin of microglial and perivascular cells in brain Exp. Neurol. 186 2004 134 144
14. C.P. Hofstetter, E.J. Schwarz, D. Hess, J. Widenfalk, A. El Manira, D.J. Prockop, and L. Olson Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery Proc. Natl. Acad. Sci. U. S. A. 99 2002 2199 2204
15. J.E. Hudson, N. Chen, S. Song, P. Walczak, P. Jendelova, E. Sykova, A.E. Willing, S. Saporta, P. Bickford, J. Sanchez-Ramos, and T. Zigova Green fluorescent protein bone marrow cells express hematopoietic and neural antigens in culture and migrate within the neonatal rat brain J. Neurosci. Res. 76 2004 255 264
16. S.C. Hung, H. Cheng, C.Y. Pan, M.J. Tsai, L.S. Kao, and H.L. Ma In vitro differentiation of size-sieved stem cells into electrically active neural cells Stem Cells 20 2002 522 529
17. Y. Jiang, B.N. Jahagirdar, R.L. Reinhardt, R.E. Schwartz, C.D. Keene, X.R. Ortiz-Gonzalez, M. Reyes, T. Lenvik, T. Lund, M. Blackstad, J. Du, S. Aldrich, A. Lisberg, W.C. Low, D.A. Largaespada, and C.M. Verfaillie Pluripotency of mesenchymal stem cells derived from adult marrow Nature 418 2002 41 49
18. Y. Jiang, D. Henderson, M. Blackstad, A. Chen, R.F. Miller, and C.M. Verfaillie Neuroectodermal differentiation from mouse multipotent adult progenitor cells Proc. Natl. Acad. Sci. U. S. A. 100 Suppl. 1 2003 11854 11860
19. K. Jin, X.O. Mao, S. Batteur, Y. Sun, and D.A. Greenberg Induction of neuronal markers in bone marrow cells: differential effects of growth factors and patterns of intracellular expression Exp. Neurol. 184 2003 78 89
20. A. Joannides, P. Gaughwin, M. Scott, S. Watt, A. Compston, and S. Chandran Postnatal astrocytes promote neural induction from adult human bone marrow-derived stem cells J. Hematother. Stem Cell Res. 12 2003 681 688
21. P. Kabos, M. Ehtesham, A. Kabosova, K.L. Black, and J.S. Yu Generation of neural progenitor cells from whole adult bone marrow Exp. Neurol. 178 2002 288 293
22. E.R. Kandel, J.H. Schwartz, and T.M. Jessell Principles of neural science 2000 McGraw-Hill New York
23. B.J. Kim, J.H. Seo, J.K. Bubien, and Y.S. Oh Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro Neuroreport 13 2002 1185 1188
24. J. Kohyama, H. Abe, T. Shimazaki, A. Koizumi, K. Nakashima, S. Gojo, T. Taga, H. Okano, J. Hata, and A. Umezawa Brain from bone: efficient "meta-differentiation" of marrow stroma-derived mature osteoblasts to neurons with Noggin or a demethylating agent Differentiation 68 2001 235 244
25. G.C. Kopen, D.J. Prockop, and D.G. Phinney Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains Proc. Natl. Acad. Sci. U. S. A. 96 1999 10711 10716
26. S. Koshizuka, S. Okada, A. Okawa, M. Koda, M. Murasawa, M. Hashimoto, T. Kamada, K. Yoshinaga, M. Murakami, H. Moriya, and M. Yamazaki Transplanted hematopoietic stem cells from bone marrow differentiate into neural lineage cells and promote functional recovery after spinal cord injury in mice J. Neuropathol. Exp. Neurol. 63 2004 64 72
27. S.H. Lee, N. Lumelsky, L. Studer, J.M. Auerbach, and R.D. McKay Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells Nat. Biotechnol. 18 2000 675 679
28. U. Lendahl, L.B. Zimmerman, and R.D. McKay CNS stem cells express a new class of intermediate filament protein Cell 60 1990 585 595
29. Y.S. Levy, D. Merims, H. Panet, Y. Barhum, E. Melamed, and D. Offen Induction of neuron-specific enolase promoter and neuronal markers in differentiated mouse bone marrow stromal cells J. Mol. Neurosci. 21 2003 121 132
30. Y. Liu, and M.S. Rao Transdifferentiation-fact or artifact J. Cell. Biochem. 88 2003 29 40
31. F. Locatelli, S. Corti, C. Donadoni, M. Guglieri, F. Capra, S. Strazzer, S. Salani, R. Del Bo, F. Fortunato, A. Bordoni, and G.P. Comi Neuronal differentiation of murine bone marrow Thy-1- and Sca-1-positive cells J. Hematother. Stem Cell Res. 12 2003 727 734
32. P. Lu, A. Blesch, and M.H. Tuszynski Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J. Neurosci. Res. 77 2004 174 191
33. P. Lu, L.L. Jones, and M.H. Tuszynski BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury Exp. Neurol. 191 2005 344 360
34. W. Ma, W. Fitzgerald, Q.Y. Liu, T.J. O'Shaughnessy, D. Maric, H.J. Lin, D.L. Alkon, and J.L. Barker CNS stem and progenitor cell differentiation into functional neuronal circuits in three-dimensional collagen gels Exp. Neurol. 190 2004 276 288
35. M. Mayer-Proschel, A.J. Kalyani, T. Mujtaba, and M.S. Rao Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells Neuron 19 1997 773 785
36. E. Mezey, K.J. Chandross, G. Harta, R.A. Maki, and S.R. McKercher Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow Science 290 2000 1779 1782
37. E. Mezey, S. Key, G. Vogelsang, I. Szalayova, G.D. Lange, and B. Crain Transplanted bone marrow generates new neurons in human brains Proc. Natl. Acad. Sci. U. S. A. 100 2003 1364 1369
38. G.B. Miles, D.C. Yohn, H. Wichterle, T.M. Jessell, V.F. Rafuse, and R.M. Brownstone Functional properties of motoneurons derived from mouse embryonic stem cells J. Neurosci. 24 2004 7848 7858
39. G. Munoz-Elias, D. Woodbury, and I.B. Black Marrow stromal cells, mitosis, and neuronal differentiation: stem cell and precursor functions Stem Cells 21 2003 437 448
40. G. Munoz-Elias, A.J. Marcus, T.M. Coyne, D. Woodbury, and I.B. Black Adult bone marrow stromal cells in the embryonic brain: engraftment, migration, differentiation, and long-term survival J. Neurosci. 24 2004 4585 4595
41. K. Nakano, M. Migita, H. Mochizuki, and T. Shimada Differentiation of transplanted bone marrow cells in the adult mouse brain Transplantation 71 2001 1735 1740
42. B. Neuhuber, G. Gallo, L. Howard, L. Kostura, A. Mackay, and I. Fischer Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype J. Neurosci. Res. 77 2004 192 204
43. S. Okabe, K. Forsberg-Nilsson, A.C. Spiro, M. Segal, and R.D. McKay Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro Mech. Dev. 59 1996 89 102
44. K. Ono, K. Yoshihara, H. Suzuki, K.F. Tanaka, T. Takii, K. Onozaki, and M. Sawada Preservation of hematopoietic properties in transplanted bone marrow cells in the brain J. Neurosci. Res. 72 2003 503 507
45. C.S. Padovan, K. Jahn, T. Birnbaum, P. Reich, P. Sostak, M. Strupp, and A. Straube Expression of neuronal markers in differentiated marrow stromal cells and CD133+ stem-like cells Cell Transplant 12 2003 839 848
46. J. Priller, D.A. Persons, F.F. Klett, G. Kempermann, G.W. Kreutzberg, and U. Dirnagl Neogenesis of cerebellar Purkinje neurons from gene-marked bone marrow cells in vivo J. Cell Biol. 155 2001 733 738
47. M.Z. Ratajczak, M. Kucia, R. Reca, M. Majka, A. Janowska-Wieczorek, and J. Ratajczak Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells 'hide out' in the bone marrow Leukemia 18 2004 29 40
48. J.G. Reeve, J. Stewart, J.V. Watson, D. Wulfrank, P.R. Twentyman, and N.M. Bleehen Neuron specific enolase expression in carcinoma of the lung Br. J. Cancer 53 1986 519 528
49. N. Rismanchi, C.L. Floyd, R.F. Berman, and B.G. Lyeth Cell death and long-term maintenance of neuron-like state after differentiation of rat bone marrow stromal cells: a comparison of protocols Brain Res. 991 2003 46 55
50. J. Sanchez-Ramos, S. Song, F. Cardozo-Pelaez, C. Hazzi, T. Stedeford, A. Willing, T.B. Freeman, S. Saporta, W. Janssen, N. Patel, D.R. Cooper, and P.R. Sanberg Adult bone marrow stromal cells differentiate into neural cells in vitro Exp. Neurol. 164 2000 247 256
51. G. Sjoberg, W.Q. Jiang, N.R. Ringertz, U. Lendahl, and T. Sejersen Colocalization of nestin and vimentin/desmin in skeletal muscle cells demonstrated by three-dimensional fluorescence digital imaging microscopy Exp. Cell Res. 214 1994 447 458
52. H.J. Song, C.F. Stevens, and F.H. Gage Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons Nat. Neurosci. 5 2002 438 445
53. H. Suzuki, T. Taguchi, H. Tanaka, H. Kataoka, Z. Li, K. Muramatsu, T. Gondo, and S. Kawai Neurospheres induced from bone marrow stromal cells are multipotent for differentiation into neuron, astrocyte, and oligodendrocyte phenotypes Biochem. Biophys. Res. Commun. 322 2004 918 922
54. J. Takahashi, T.D. Palmer, and F.H. Gage Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures J. Neurobiol. 38 1999 65 81
55. N. Terada, T. Hamazaki, M. Oka, M. Hoki, D.M. Mastalerz, Y. Nakano, E.M. Meyer, L. Morel, B.E. Petersen, and E.W. Scott Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion Nature 416 2002 542 545
56. A.V. Terskikh, M.C. Easterday, L. Li, L. Hood, H.I. Kornblum, D.H. Geschwind, and I.L. Weissman From hematopoiesis to neuropoiesis: evidence of overlapping genetic programs Proc. Natl. Acad. Sci. U. S. A. 98 2001 7934 7939
57. T. Tondreau, L. Lagneaux, M. Dejeneffe, M. Massy, C. Mortier, A. Delforge, and D. Bron Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation Differentiation 72 2004 319 326
58. W. Vogel, F. Grunebach, C.A. Messam, L. Kanz, W. Brugger, and H.J. Buhring Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells Haematologica 88 2003 126 133
59. P. Walczak, N. Chen, J.E. Hudson, A.E. Willing, S.N. Garbuzova-Davis, S. Song, P.R. Sanberg, J. Sanchez-Ramos, P.C. Bickford, and T. Zigova Do hematopoietic cells exposed to a neurogenic environment mimic properties of endogenous neural precursors? J. Neurosci. Res. 76 2004 244 254
60. J.M. Weimann, C.A. Charlton, T.R. Brazelton, R.C. Hackman, and H.M. Blau Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains Proc. Natl. Acad. Sci. U. S. A. 100 2003 2088 2093
61. J.M. Weimann, C.B. Johansson, A. Trejo, and H.M. Blau Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant Nat. Cell Biol. 5 2003 959 966
62. U. Westerlund, M.C. Moe, M. Varghese, J. Berg-Johnsen, M. Ohlsson, I.A. Langmoen, and M. Svensson Stem cells from the adult human brain develop into functional neurons in culture Exp. Cell Res. 289 2003 378 383
63. D. Woodbury, E.J. Schwarz, D.J. Prockop, and I.B. Black Adult rat and human bone marrow stromal cells differentiate into neurons J. Neurosci. Res. 61 2000 364 370
64. D. Woodbury, K. Reynolds, and I.B. Black Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis J. Neurosci. Res. 69 2002 908 917
65. Q.L. Ying, J. Nichols, E.P. Evans, and A.G. Smith Changing potency by spontaneous fusion Nature 416 2002 545 548
66. L.R. Zhao, W.M. Duan, M. Reyes, C.D. Keene, C.M. Verfaillie, and W.C. Low Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats Exp. Neurol. 174 2002 11 20