Mesenchymal Stem Cells Stimulate Endogenous Neurogenesis in the Subventricular Zone of Adult Mice

Stem Cell Reviews and Reports

Volumn 7, Issue 2, 2011, Pages 404-412

  Kan, Inna ^a   Barhum, Yael ^a   Melamed, Eldad ^a   Offen, Daniel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Adult stem cell; Brain derived neurotrophic factor; Cell transplantation; Enriched environment; Neural stem cell; Neurogenesis; Subgranular zone; Subventricular zone

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NUCLEAR PROTEIN;

ANIMAL; ARTICLE; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; FEMALE; HIPPOCAMPUS; HUMAN; LATERAL BRAIN VENTRICLE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SECRETION; XENOGRAFT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; HIPPOCAMPUS; HUMANS; LATERAL VENTRICLES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; NUCLEAR PROTEINS; TRANSPLANTATION, HETEROLOGOUS;

MAMMALIA; MUS;

EID: 79954999836     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-010-9190-x     Document Type: Article

References (55)

1. Garcia-Verdugo, J. M., Doetsch, F., Wichterle, H., Lim, D. A., & varez-Buylla, A. (1998). Architecture and cell types of the adult subventricular zone: in search of the stem cells. Journal of Neurobiology, 36(2), 234-248.
2. Zhao, C., Deng, W., & Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4), 645-660.
3. Suh, H., Deng, W., & Gage, F. H. (2009). Signaling in adult neurogenesis. Annual Review of Cell and Developmental Biology, 25, 253-275.
4. Bordey, A. (2006). Adult neurogenesis: basic concepts of signaling. Cell Cycle, 5(7), 722-728.
5. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M., & varez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97(6), 703-716.
6. Morshead, C. M., Reynolds, B. A., Craig, C. G., McBurney, M. W., Staines, W. A., Morassutti, D., et al. (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron, 13(5), 1071-1082.
7. Seri, B., Garcia-Verdugo, J. M., Collado-Morente, L., McEwen, B. S., & varez-Buylla, A. (2004). Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. The Journal of Comparative Neurology, 478(4), 359-378.
8. Ahn, S., & Joyner, A. L. (2005). In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature, 437(7060), 894-897.
9. Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., & Cameron, H. A. (2003). Short-term and long-term survival of new neurons in the rat dentate gyrus. The Journal of Comparative Neurology, 460(4), 563-572.
10. Lie, D. C., Song, H., Colamarino, S. A., Ming, G. L., & Gage, F. H. (2004). Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annual Review of Pharmacology and Toxicology, 44, 399-421.
11. Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature, 386(6624), 493-495.
12. Kempermann, G., Kuhn, H. G., & Gage, F. H. (1998). Experience-induced neurogenesis in the senescent dentate gyrus. The Journal of Neuroscience, 18(9), 3206-3212.
13. Kempermann, G., Gast, D., & Gage, F. H. (2002). Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Annals of Neurology, 52(2), 135-143.
14. Brown, J., Cooper-Kuhn, C. M., Kempermann, G., Van, P. H., Winkler, J., Gage, F. H., et al. (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. The European Journal of Neuroscience, 17(10), 2042-2046.
15. Ehninger, D., & Kempermann, G. (2003). Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cerebral Cortex, 13(8), 845-851.
16. van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of environmental enrichment. Nature Reviews Neuroscience, 1(3), 191-198.
17. Nithianantharajah, J., & Hannan, A. J. (2006). Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature Reviews. Neuroscience, 7(9), 697-709.
18. Owen, M., & Friedenstein, A. J. (1988). Stromal stem cells: marrow-derived osteogenic precursors. Ciba Foundation Symposium, 136, 42-60.
19. Prockop, D. J. (1997). Marrow stromal cells as stem cells for nonhematopoietic tissues. Science, 276(5309), 71-74.
20. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., et al. (1999). Multilineage potential of adult human mesenchymal stem cells. Science, 284(5411), 143-147.
21. Zipori, D. (2004). Mesenchymal stem cells: harnessing cell plasticity to tissue and organ repair. Blood Cells, Molecules & Diseases, 33(3), 211-215.
22. Pittenger, M. F., & Martin, B. J. (2004). Mesenchymal stem cells and their potential as cardiac therapeutics. Circulation Research, 95(1), 9-20.
23. Lee, R. H., Seo, M. J., Reger, R. L., Spees, J. L., Pulin, A. A., Olson, S. D., et al. (2006). Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. PNAS, 103(46), 17438-17443.
24. Rojas, M., Xu, J., Woods, C. R., Mora, A. L., Spears, W., Roman, J., et al. (2005). Bone marrow-derived mesenchymal stem cells in repair of the injured lung. American Journal of Respiratory Cell and Molecular Biology, 33(2), 145-152.
25. Le, B. K., Rasmusson, I., Sundberg, B., Gotherstrom, C., Hassan, M., Uzunel, M., et al. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 363(9419), 1439-1441.
26. Chen, J., Li, Y., Wang, L., Zhang, Z., Lu, D., Lu, M., et al. (2001). Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke, 32(4), 1005-1011.
27. Chopp, M., Zhang, X. H., Li, Y., Wang, L., Chen, J., Lu, D., et al. (2000). Spinal cord injury in rat: treatment with bone marrow stromal cell transplantation. NeuroReport, 11(13), 3001-3005.
28. Mahmood, A., Lu, D., Lu, M., & Chopp, M. (2003). Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery, 53(3), 697-702.
29. Kan, I., Melamed, E., & Offen, D. (2007). Autotransplantation of bone marrow-derived stem cells as a therapy for neurodegenerative diseases. Handbook of Experimental Pharmacology, 180, 219-242.
30. Phinney, D. G., & Prockop, D. J. (2007). Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells, 25(11), 2896-2902.
31. Paxinos, G., & Franklin, K. B. J. (2004). The mouse brain in stereotaxic coordinates. San Diego: Academic.
32. Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., et al. (2006). Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nature Neuroscience, 9(2), 268-275.
33. Tremain, N., Korkko, J., Ibberson, D., Kopen, G. C., DiGirolamo, C., & 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(5), 408-418.
34. Li, Y., Chen, J., Chen, X. G., Wang, L., Gautam, S. C., Xu, Y. X., et al. (2002). Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology, 59(4), 514-523.
35. Chen, Q., Long, Y., Yuan, X., Zou, L., Sun, J., Chen, S., et al. (2005). Protective effects of bone marrow stromal cell transplantation in injured rodent brain: synthesis of neurotrophic factors. Journal of Neuroscience Research, 80(5), 611-619.
36. Crigler, L., Robey, R. C., Asawachaicharn, A., Gaupp, D., & Phinney, D. G. (2006). Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Experimental Neurology, 198(1), 54-64.
37. Mullen, R. J., Buck, C. R., & Smith, A. M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116(1), 201-211.
38. Yoo, S. W., Kim, S. S., Lee, S. Y., Lee, H. S., Kim, H. S., Lee, Y. D., et al. (2008). Mesenchymal stem cells promote proliferation of endogenous neural stem cells and survival of newborn cells in a rat stroke model. Experimental & Molecular Medicine, 40(4), 387-397.
39. Cova, L., Armentero, M. T., Zennaro, E., Calzarossa, C., Bossolasco, P., Busca, G., et al. (2010). Multiple neurogenic and neurorescue effects of human mesenchymal stem cell after transplantation in an experimental model of Parkinson's disease. Brain Research, 1311, 12-27.
40. Munoz, J. R., Stoutenger, B. R., Robinson, A. P., Spees, J. L., & Prockop, D. J. (2005). Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. PNAS, 102(50), 18171-18176.
41. Tfilin, M., Sudai, E., Merenlender, A., Gispan, I., Yadid, G., & Turgeman, G. (2009). Mesenchymal stem cells increase hippocampal neurogenesis and counteract depressive-like behavior. Molecular Psychiatry. doi: 10. 1038/mp. 2009. 110.
42. Lim, D. A., Tramontin, A. D., Trevejo, J. M., Herrera, D. G., Garcia-Verdugo, J. M., & Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron, 28(3), 713-726.
43. Zigova, T., Pencea, V., Wiegand, S. J., & Luskin, M. B. (1998). Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Molecular and Cellular Neuroscience, 11(4), 234-245.
44. Pencea, V., Bingaman, K. D., Wiegand, S. J., & Luskin, M. B. (2001). Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. The Journal of Neuroscience, 21(17), 6706-6717.
45. Benraiss, A., Chmielnicki, E., Lerner, K., Roh, D., & Goldman, S. A. (2001). Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. The Journal of Neuroscience, 21(17), 6718-6731.
46. Chmielnicki, E., Benraiss, A., Economides, A. N., & Goldman, S. A. (2004). Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. The Journal of Neuroscience, 24(9), 2133-2142.
47. Galvao, R. P., Garcia-Verdugo, J. M., & Alvarez-Buylla, A. (2008). Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. The Journal of Neuroscience, 28(50), 13368-13383.
48. Xu, G., Zhang, L., Ren, G., Yuan, Z., Zhang, Y., Zhao, R. C., et al. (2007). Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Research, 17(3), 240-248.
49. Le Blanc, K., Frassoni, F., Ball, L., Locatelli, F., Roelofs, H., Lewis, I., et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet, 371(9624), 1579-1586.
50. Burt, R. K., Loh, Y., Pearce, W., Beohar, N., Barr, W. G., Craig, R., et al. (2008). Clinical applications of blood-derived and marrow-derived stem cells for nonmalignant diseases. Journal of the American Medical Association, 299(8), 925-936.
51. Parekkadan, B., Tilles, A. W., & Yarmush, M. L. (2008). Bone marrow-derived mesenchymal stem cells ameliorate autoimmune enteropathy independent of regulatory T cells. Stem Cells, 26(7), 1913-1919.
52. Ren, G., Zhang, L., Zhao, X., Xu, G., Zhang, Y., Roberts, A. I., et al. (2008). Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell, 2(2), 141-150.
53. Ryan, J., Barry, F., Murphy, J. M., & Mahon, B. (2005). Mesenchymal stem cells avoid allogeneic rejection. Journal of Inflammation. doi: 10. 1186/1476-9255-2-8.
54. Zhang, J., Li, Y., Chen, J., Cui, Y., Lu, M., Elias, S. B., et al. (2005). Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Experimental Neurology, 195(1), 16-26.
55. Rossignol, J., Boyer, C., Thinard, R., Remy, S., Dugast, A. S., Dubayle, D., et al. (2009). Mesenchymal stem cells induce a weak immune response in the rat striatum after allo or xenotransplantation. Journal of Cellular and Molecular Medicine, 13(8B), 2547-2558.