Survival and neuronal differentiation of mesenchymal stem cells transplanted into the rodent brain are dependent upon microenvironment

Tissue Engineering - Part A

Volumn 16, Issue 9, 2010, Pages 2769-2782

  Lepski, Guilherme ^a,c   Jannes, Cinthia E ^b   Strauss, Bryan ^b   Marie, Suely K N ^b   Nikkhah, Guido ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL DEATH; CELL PROLIFERATION; ELECTROPHYSIOLOGY; FETAL MONITORING; FLOWCHARTING; FLUORESCENCE; NEURONS; PROTEINS; RATS; STEM CELLS;

ADULT BRAIN; CELL DEGENERATION; CELL SUSPENSION; CENTRAL NERVOUS SYSTEMS; CULTURE MEDIUM; CYCLIC ADENOSINE; GREEN FLUORESCENT PROTEIN; IN-VITRO; IN-VIVO; IONIC CHANNELS; ISOLATED CELLS; MESENCHYMAL STEM CELL; MICROENVIRONMENTS; MICROTUBULE ASSOCIATED PROTEIN; NEUROFILAMENTS; NEURONAL DIFFERENTIATION; NEURONAL MARKERS; NUCLEAR PROTEINS; RODENT BRAIN; STRIATUM;

CELL CULTURE;

ANIMALIA; LENTIVIRUS; RATTUS; RODENTIA;

CYCLIC AMP;

ANIMAL; ARTICLE; BRAIN; CELL CULTURE; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; CYTOLOGY; ELECTROPHYSIOLOGY; GENETICS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; METHODOLOGY; NERVE CELL; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIC AMP; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICROSCOPY, CONFOCAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77956089123     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0686     Document Type: Article

References (54)

1. Sanchez-Ramos, J., Song, S., Cardozo-Pelaez, F., Hazzi, C., Stedeford, T., Willing, A., Freeman, T.B., Saporta, S., Janssen, W., Patel, N., Cooper, D.R., and Sanberg, P.R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164, 247, 2000.
2. 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, 364, 2000.
3. Lepski, G., Jannes, C.E., Maciaczyk, J., Papazoglou, A., Mehlhorn, A.T., Kaiser, S., Teixeira, M.J., Marie, S.K., Bis-chofberger, J., and Nikkhah, G. Limited Ca(2\+) and PKA-pathway dependent neurogenic differentiation of human adult mesenchymal stem cells as compared to fetal neuronal stem cells. Exp Cell Res 316, 216, 2010.
4. Hofstetter, C.P., Schwarz, E.J., Hess, D., Widenfalk, J., El, M.A., Prockop, D.J., and Olson, L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci USA 99, 2199, 2002.
5. Hess, D.C., Hill, W.D., Martin-Studdard, A., Carroll, J., Brailer, J., and Carothers, J. Bone marrow as a source of endothelial cells and NeuN-expressing cells After stroke. Stroke 33, 1362, 2002.
6. Kim, S.S., Yoo, S.W., Park, T.S., Ahn, S.C., Jeong, H.S., Kim, J.W., Chang, D.Y., Cho, K.G., Kim, S.U., Huh, Y., Lee, J.E., Lee, S.Y., Lee, Y.D., and Suh-Kim, H. Neural induction with neurogenin1 increases the therapeutic effects of mesenchymal stem cells in the ischemic brain. Stem Cells 26, 2217, 2008.
7. Akiyama, Y., Radtke, C., and Kocsis, J.D. Remyelination of the rat spinal cord by transplantation of identified bone marrow stromal cells. J Neurosci 22, 6623, 2002.
8. 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 USA 95, 3908, 1998.
9. Pittenger, M.F., Mackay, 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. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
10. Nikkhah, G., Olsson, M., Eberhard, J., Bentlage, C., Cunningham, M.G., and Bjorklund, A. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63, 57, 1994.
11. Nikkhah, G., Rosenthal, C., Falkenstein, G., Roedter, A., Papazoglou, A., and Brandis, A. Microtransplantation of dopaminergic cell suspensions: further characterization and optimization of grafting parameters. Cell Transplant. 18, 119, 2009.
12. Kempermann, G., Kuhn, H.G., and Gage, F.H. More hip-pocampal neurons in adult mice living in an enriched environment. Nature 386, 493, 1997.
13. Kempermann, G., Gast, D., and Gage, F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52, 135, 2002.
14. Van, P.H., Kempermann, G., and Gage, F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2, 266, 1999.
15. Van, P.H., Kempermann, G., and Gage, F.H. Neural consequences of environmental enrichment. Nat Rev Neurosci 1, 191, 2000.
16. Bentlage, C., Nikkhah, G., Cunningham, M.G., and Bjorklund, A. Reformation of the nigrostriatal pathway by fetal dopami-nergic micrografts into the substantia nigra is critically dependent on the age of the host. Exp Neurol 159, 177, 1999.
17. Falkenstein, G., Rosenthal, C., Reum, T., Morgenstern, R., Dobrossy, M., and Nikkhah, G. Pattern of long-term senso-rimotor recovery following intrastriatal and\accumbens DA micrografts in a rat model of Parkinson's disease. J Comp Neurol 515, 41, 2009.
18. Roedter, A., Winkler, C., Samii, M., Walter, G.F., Brandis, A., and Nikkhah, G. Comparison of unilateral and bilateral in-trastriatal 6-hydroxydopamine-induced axon terminal lesions: evidence for interhemispheric functional coupling of the two nigrostriatal pathways. J Comp Neurol 432, 217, 2001.
19. Winkler, C., Bentlage, C., Nikkhah, G., Samii, M., and Bjorklund, A. Intranigral transplants of GABA-rich striatal tissue induce behavioral recovery in the rat Parkinson model and promote the effects obtained by intrastriatal dopami-nergic transplants. Exp Neurol 155, 165, 1999.
20. Kang, T.J., Yeom, J.E., Lee, H.J., Rho, S.H., Han, H., and Chae, G.T. Growth kinetics of human mesenchymal stem cells from bone marrow and umbilical cord blood. Acta Haematol 112, 230, 2004.
21. Mezey, E., Key, S., Vogelsang, G., Szalayova, I., Lange, G.D., and Crain, B. Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci USA 100, 1364, 2003.
22. Greco, S.J., Zhou, C., Ye, J.H., and Rameshwar, P. An interdisciplinary approach and characterization of neuronal cells transdifferentiated from human mesenchymal stem cells. Stem Cells Dev 16, 811, 2007.
23. Khoo, M.L., Shen, B., Tao, H., and Ma, D.D. Long-term serial passage and neuronal differentiation capability of human bone marrow mesenchymal stem cells. Stem Cells Dev 17, 883, 2008.
24. Kim, B.J., Seo, J.H., Bubien, J.K., and Oh, Y.S. Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro. Neuroreport 13, 1185, 2002.
25. Trzaska, K.A., Reddy, B.Y., Munoz, J.L., Li, K.Y., Ye, J.H., and Rameshwar, P. Loss of RE-1 silencing factor in mesen-chymal stem cell-derived dopamine progenitors induces functional maturity. Mol Cell Neurosci 39, 285, 2008.
26. Lu, P., Blesch, A., and Tuszynski, M.H. Induction of bone marrow stromal cells to neurons: differentiation, transdif-ferentiation, or artifact? J Neurosci Res 77, 174, 2004.
27. Neuhuber, B., Gallo, G., Howard, L., Kostura, L., Mackay, A., and Fischer, I. 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, 192, 2004.
28. Hermann, A., Liebau, S., Gastl, R., Fickert, S., Habisch, H.J., Fiedler, J., Schwarz, J., Brenner, R., and Storch, A. Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J Neurosci Res 83, 1502, 2006.
29. Lee, J., Elkahloun, A.G., Messina, S.A., Ferrari, N., Xi, D., Smith, C.L., Cooper, R., Jr., Albert, P.S., and Fine, H.A. Cellular and genetic characterization of human adult bone marrow-derived neural stem-like cells: a potential anti-glioma cellular vector. Cancer Res 63, 8877, 2003.
30. Woodbury, D., Reynolds, K., and Black, I.B. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res 69, 908, 2002.
31. Fu, L., Zhu, L., Huang, Y., Lee, T.D., Forman, S.J., and Shih, C.C. Derivation of neural stem cells from mesenchymal stemcells: evidence for a bipotential stem cell population. Stem Cells Dev 17, 1109, 2008.
32. Song, H., Stevens, C.F., and Gage, F.H. Astroglia induce neu-rogenesis from adult neural stem cells. Nature 417, 39, 2002.
33. Song, H.J., Stevens, C.F., and Gage, F.H. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5, 438, 2002.
34. Choi, C.B., Cho, Y.K., Prakash, K.V., Jee, B.K., Han, C.W., Paik, Y.K., Kim, H.Y., Lee, K.H., Chung, N., and Rha, H.K. Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochem Biophys Res Com-mun 350, 138, 2006.
35. Coppi, E., Pugliese, A.M., Urbani, S., Melani, A., Cerbai, E., Mazzanti, B., Bosi, A., Saccardi, R., and Pedata, F. ATP modulates cell proliferation and elicits two different elec-trophysiological responses in human mesenchymal stem cells. Stem Cells 25, 1840, 2007.
36. Heubach, J.F., Graf, E.M., Leutheuser, J., Bock, M., Balana, B., Zahanich, I., Christ, T., Boxberger, S., Wettwer, E., and Ravens, U. Electrophysiological properties of human mes-enchymal stem cells. J Physiol 554, 659, 2004.
37. Li, G.R., Deng, X.L., Sun, H., Chung, S.S., Tse, H.F., and Lau, C.P. Ion channels in mesenchymal stem cells from rat bone marrow. Stem Cells 24, 1519, 2006.
38. Wenisch, S., Trinkaus, K., Hild, A., Hose, D., Heiss, C., Alt, V., Klisch, C., Meissl, H., and Schnettler, R. Immunochemical, ultrastructural and electrophysiological investigations of bone-derived stem cells in the course of neuronal differentiation. Bone 38, 911, 2006.
39. Yang, C.C., Shih, Y.H., Ko, M.H., Hsu, S.Y., Cheng, H., and Fu, Y.S. Transplantation of human umbilical mesenchymal stem cells from Wharton's jelly after complete transection of the rat spinal cord. PLoS ONE 3, e3336, 2008.
40. Bai, L., Caplan, A., Lennon, D., and Miller, R.H. Human mesenchymal stem cells signals regulate neural stem cell fate. Neurochem Res 32, 353, 2007.
41. Cizkova, D., Rosocha, J., Vanicky, I., Jergova, S., and Cizek, M. Transplants of human mesenchymal stem cells improve functional recovery after spinal cord injury in the rat. Cell Mol Neurobiol 26, 1167, 2006.
42. Cizkova, D., Kakinohana, O., Kucharova, K., Marsala, S., Johe, K., Hazel, T., Hefferan, M.P., and Marsala, M. Functional recovery in rats with ischemic paraplegia after spinal grafting of human spinal stem cells. Neuroscience 147, 546, 2007.
43. Zwart, I., Hill, A.J., Al-Allaf, F., Shah, M., Girdlestone, J., Sanusi, A.B., Mehmet, H., Navarrete, R., Navarrete, C., and Jen, L.S. Umbilical cord blood mesenchymal stromal cells are neuroprotective and promote regeneration in a rat optic tract model. Exp Neurol 216, 439, 2009.
44. Liu, C.T., Yang, Y.J., Yin, F., Wang, X., Yu, X.H., Wang, Q.H., Wang, X.L., and Xie, M. The immunobiological development of human bone marrow mesenchymal stem cells in the course of neuronal differentiation. Cell Immunol 244, 19, 2006.
45. Luzzati, F., De, M.S., Fasolo, A., and Peretto, P. Adult neu-rogenesis and local neuronal progenitors in the striatum. Neurodegener Dis 4, 322, 2007.
46. Maciaczyk, J., Singec, I., Maciaczyk, D., Klein, A., and Nik-khah, G. Restricted spontaneous in vitro differentiation and region-specific migration of long-term expanded fetal human neural precursor cells after transplantation into the adult rat brain. Stem Cells Dev 18, 1043, 2009.
47. Seki, T. Microenvironmental elements supporting adult hippocampal neurogenesis. Anat Sci Int 78, 69, 2003.
48. Ge, S., Goh, E.L., Sailor, K.A., Kitabatake, Y., Ming, G.L., and Song, H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589, 2006.
49. Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184, 2004.
50. Tozuka, Y., Fukuda, S., Namba, T., Seki, T., and Hisatsune, T. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803, 2005.
51. Ma, D.K., Ming, G.L., and Song, H. Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr Opin Neurobiol 15, 514, 2005.
52. Lie, D.C., Colamarino, S.A., Song, H.J., Desire, L., Mira, H., Consiglio, A., Lein, E.S., Jessberger, S., Lansford, H., Dearie, A.R., and Gage, F.H. Wnt signalling regulates adult hippo-campal neurogenesis. Nature 437, 1370, 2005.
53. Bjorklund, A. and Stenevi, U. Reconstruction of the nigros-triatal dopamine pathway by intracerebral nigral transplants. Brain Res 177, 555, 1979.
54. Kromer, L.F., Bjorklund, A., and Stenevi, U. Intracephalic implants: a technique for studying neuronal interactions. Science 204, 1117, 1979.