Neurotrophin-directed differentiation of human adult marrow stromal cells to dopaminergic-like neurons

Bone

Volumn 40, Issue 2, 2007, Pages 360-373

  Tatard, Valerie M ^a   D'Ippolito, Gianluca ^b,d   Diabira, Sylma ^a,b   Valeyev, Alexander ^c,d   Hackman, John ^c,d   McCarthy, Micheline ^c,d   Bouckenooghe, Thomas ^a   Menei, Philippe ^a   Montero Menei, Claudia N ^a   Schiller, Paul C ^b,c,d  

^a ANGERS UNIVERSITY HOSPITAL   (France)

^b Geriatric Research Education   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

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

Author keywords

Bone marrow; Differentiation; Dopamine; Neurotrophin 3; Stem cell

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BETA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CELL MARKER; CLASS 3 BETA TUBULIN; FIBROBLAST GROWTH FACTOR 8; GLIAL FIBRILLARY ACIDIC PROTEIN; NERVE GROWTH FACTOR; NESTIN; NEUROFILAMENT L; NEUROFILAMENT M; NEUROFILAMENT PROTEIN; NEURON SPECIFIC ENOLASE; NEURONAL NUCLEAR PROTEIN NEUN; NEUROTROPHIN; NEUROTROPIN 3; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE A; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGE; AGED; ARTICLE; BONE DISEASE; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CHILD; CONTROLLED STUDY; CULTURE MEDIUM; DEPOLARIZATION; DOPAMINERGIC LIKE NERVE CELL; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; FEMALE; FETUS; HUMAN; HUMAN CELL; MALE; MARROW ISOLATED ADULT MULTILINEAGE INDUCIBLE CELL; NERVE FIBER GROWTH; NEUROLOGIC DISEASE; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGENERATIVE MEDICINE; STEM CELL; STEM CELL TRANSPLANTATION;

ADOLESCENT; ADULT; ADULT STEM CELLS; AGE FACTORS; AGED; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; DOPAMINE; FEMALE; FIBROBLAST GROWTH FACTOR 8; HEDGEHOG PROTEINS; HUMANS; MALE; MIDDLE AGED; NEURITES; NEURONS; NEUROTROPHIN 3; RECOMBINANT PROTEINS; STROMAL CELLS; TRETINOIN; TYROSINE 3-MONOOXYGENASE;

EID: 33846169731     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2006.09.013     Document Type: Article

References (56)

1. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
2. Colter D.C., Sekiya I., and Prockop D.J. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 7841-7845
3. D'Ippolito G., Schiller P.C., Ricordi C., Roos B.A., and Howard G.A. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J. Bone Miner. Res. 14 (1999) 1115-1122
4. Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276 (1997) 71-74
5. Caplan A.I. Mesenchymal stem cells. J. Orthop. Res. 9 (1991) 641-650
6. Reyes M., and Verfaillie C.M. Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann. N. Y. Acad. Sci. 938 (2001) 231-233 (discussion 233-5)
7. D'Ippolito G., Diabira S., Howard G.A., Menei P., Roos B.A., and Schiller P.C. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J. Cell. Sci. 117 (2004) 2971-2981
8. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164 (2000) 247-256
9. Woodbury D., Schwarz E.J., Prockop D.J., and Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61 (2000) 364-370
10. Jiang Y., Henderson D., Blackstad M., Chen A., Miller R.F., and Verfaillie C.M. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 100 Suppl. 1 (2003) 11854-11860
11. Azizi S.A., Stokes D., Augelli B.J., DiGirolamo C., and Prockop D.J. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3908-3913
12. Brazelton T.R., Rossi F.M., Keshet G.I., and Blau H.M. From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290 (2000) 1775-1779
13. Mezey E., Chandross K.J., Harta G., Maki R.A., and McKercher S.R. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290 (2000) 1779-1782
14. Prockop D.J. Marrow stromal cells as stem cells for continual renewal of nonhematopoietic tissues and as potential vectors for gene therapy. J. Cell. Biochem. 30-31 (1998) 284-285 (Suppl.)
15. Zhao L.R., Duan W.M., Reyes M., Keene C.D., Verfaillie C.M., and Low W.C. 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
16. Chopp M., Zhang X.H., Li Y., Wang L., Chen J., Lu D., et al. Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. NeuroReport 11 (2000) 3001-3005
17. Schwarz E.J., Alexander G.M., Prockop D.J., and Azizi S.A. Multipotential marrow stromal cells transduced to produce l-DOPA: engraftment in a rat model of Parkinson disease. Hum. Gene Ther. 10 (1999) 2539-2549
18. Dezawa M., Kanno H., Hoshino M., Cho H., Matsumoto N., Itokazu Y., et al. Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. J. Clin. Invest. 113 (2004) 1701-1710
19. Tao H., Rao R., and Ma D.D. Cytokine-induced stable neuronal differentiation of human bone marrow mesenchymal stem cells in a serum/feeder cell-free condition. Dev. Growth Differ. 47 (2005) 423-433
20. Freed C.R., Breeze R.E., Rosenberg N.L., Schneck S.A., Kriek E., Qi J.X., et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease. N. Engl. J. Med. 327 (1992) 1549-1555
21. Schierle G.S., Hansson O., Leist M., Nicotera P., Widner H., and Brundin P. Caspase inhibition reduces apoptosis and increases survival of nigral transplants. Nat. Med. 5 (1999) 97-100
22. Hung S.C., Cheng H., Pan C.Y., Tsai M.J., Kao L.S., and Ma H.L. In vitro differentiation of size-sieved stem cells into electrically active neural cells. Stem Cells 20 (2002) 522-529
23. Cho K.J., Trzaska K.A., Greco S.J., McArdle J., Wang F.S., Ye J.H., et al. Neurons derived from human mesenchymal stem cells show synaptic transmission and can be induced to produce the neurotransmitter substance P by interleukin-1 alpha. Stem Cells 23 (2005) 383-391
24. Lendahl U., Zimmerman L.B., and McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell 60 (1990) 585-595
25. Cattaneo E., and McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 347 (1990) 762-765
26. Quinn S.M., Walters W.M., Vescovi A.L., and Whittemore S.R. Lineage restriction of neuroepithelial precursor cells from fetal human spinal cord. J. Neurosci. Res. 57 (1999) 590-602
27. Brewer G.J., Torricelli J.R., Evege E.K., and Price P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35 (1993) 567-576
28. Valeyev A.Y., Hackman J.C., Holohean A.M., Wood P.M., Katz J.L., and Davidoff R.A. GABA-induced Cl- current in cultured embryonic human dorsal root ganglion neurons. J. Neurophysiol. 82 (1999) 1-9
29. McCarthy M., Auger D., and Whittemore S.R. Human cytomegalovirus causes productive infection and neuronal injury in differentiating fetal human central nervous system neuroepithelial precursor cells. J. Hum. Virol. 3 (2000) 215-228
30. Taupin P., and Gage F.H. Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69 (2002) 745-749
31. McKay R. Stem cells in the central nervous system. Science 276 (1997) 66-71
32. Zimmerman L., Parr B., Lendahl U., Cunningham M., McKay R., Gavin B., et al. Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12 (1994) 11-24
33. Messam C.A., Hou J., and Major E.O. Coexpression of nestin in neural and glial cells in the developing human CNS defined by a human-specific anti-nestin antibody. Exp. Neurol. 161 (2000) 585-596
34. Cai L., Hayes N.L., and Nowakowski R.S. Synchrony of clonal cell proliferation and contiguity of clonally related cells: production of mosaicism in the ventricular zone of developing mouse neocortex. J. Neurosci. 17 (1997) 2088-2100
35. Shihabuddin L.S., Ray J., and Gage F.H. FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp. Neurol. 148 (1997) 577-586
36. Kennea N.L., and Mehmet H. Neural stem cells. J. Pathol. 197 (2002) 536-550
37. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., and van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16 (1996) 2649-2658
38. Takahashi J., Palmer T.D., and Gage F.H. Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures. J. Neurobiol. 38 (1999) 65-81
39. Barnabe-Heider F., and Miller F.D. Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J. Neurosci. 23 (2003) 5149-5160
40. Park J.K., Williams B.P., Alberta J.A., and Stiles C.D. Bipotent cortical progenitor cells process conflicting cues for neurons and glia in a hierarchical manner. J. Neurosci. 19 (1999) 10383-10389
41. Song H., Stevens C.F., and Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417 (2002) 39-44
42. Meletis K., and Frisen J. Blood on the tracks: a simple twist of fate?. Trends Neurosci 26 (2003) 292-296
43. Bertani N., Malatesta P., Volpi G., Sonego P., and Perris R. Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J. Cell. Sci. 118 (2005) 3925-3936
44. Chow D.C., Wenning L.A., Miller W.M., and Papoutsakis E.T. Modeling pO(2) distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys. J. 81 (2001) 685-696
45. Danet G.H., Pan Y., Luongo J.L., Bonnet D.A., and Simon M.C. Expansion of human SCID-repopulating cells under hypoxic conditions. J. Clin. Invest. 112 (2003) 126-135
46. Morrison S.J., White P.M., Zock C., and Anderson D.J. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96 (1999) 737-749
47. Studer L., Csete M., Lee S.H., Kabbani N., Walikonis J., Wold B., et al. Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J. Neurosci. 20 (2000) 7377-7383
48. Morrison S.J., Csete M., Groves A.K., Melega W., Wold B., and Anderson D.J. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J. Neurosci. 20 (2000) 7370-7376
49. Ye W., Shimamura K., Rubenstein J.L., Hynes M.A., and Rosenthal A. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93 (1998) 755-766
50. Simon H.H., Bhatt L., Gherbassi D., Sgado P., and Alberi L. Midbrain dopaminergic neurons: determination of their developmental fate by transcription factors. Ann. N. Y. Acad. Sci. 991 (2003) 36-47
51. Espejo M., Cutillas B., Arenas T.E., and Ambrosio S. Increased survival of dopaminergic neurons in striatal grafts of fetal ventral mesencephalic cells exposed to neurotrophin-3 or glial cell line-derived neurotrophic factor. Cell Transplant 9 (2000) 45-53
52. Baquet Z.C., Bickford P.C., and Jones K.R. Brain-derived neurotrophic factor is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta. J. Neurosci. 25 (2005) 6251-6259
53. Arenas E. Engineering a dopaminergic phenotype in stem/precursor cells: role of Nurr1, glia-derived signals, and Wnts. Ann. N. Y. Acad. Sci. 1049 (2005) 51-66
54. Kamiguchi H., Yoshida K., Sagoh M., Sasaki H., Inaba M., Wakamoto H., et al. Release of ciliary neurotrophic factor from cultured astrocytes and its modulation by cytokines. Neurochem. Res. 20 (1995) 1187-1193
55. Johe K.K., Hazel T.G., Muller T., Dugich-Djordjevic M.M., and McKay R.D. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10 (1996) 3129-3140
56. Roussa E., Farkas L.M., and Krieglstein K. TGF-beta promotes survival on mesencephalic dopaminergic neurons in cooperation with Shh and FGF-8. Neurobiol. Dis. 16 (2004) 300-310