Early passage bone marrow stromal cells express genes involved in nervous system development supporting their relevance for neural repair

Restorative Neurology and Neuroscience

Volumn 29, Issue 3, 2011, Pages 187-201

  Tewarie, R D S Nandoe ^a,b   Bossers, K ^a   Ritfeld, G J ^c,d   Blits, B ^a   Grotenhuis, J A ^b   Verhaagen, J ^a,e   Oudega, M ^d  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

BMSC; cell culture; gene profiling; microarray; stem cells

Indexed keywords

ADIPOPHILIN; CASPASE 11; CASPASE 2; CASPASE 3; CASPASE 6; CHONDROITIN SULFATE PROTEOGLYCAN 4; CLAUDIN; CLAUDIN 9; CLUSTERIN; CREATINE KINASE BB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH DIFFERENTIATION FACTOR 1; GUANINE DEAMINASE; KERATINOCYTE GROWTH FACTOR; MONOCARBOXYLATE TRANSPORTER; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; NESTIN; NUCLEAR PROTEIN; NUCLEOLAR PROTEIN 3; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEOCHONDROITIN SULFATE; PROTEOLIPID PROTEIN; PROTEOLIPID PROTEIN 2; SOMATOMEDIN C; THROMBOSPONDIN 2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG; VASCULOTROPIN C;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; BONE MARROW STROMAL CELL; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GLIA CELL; MICROARRAY ANALYSIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STROMA CELL;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD; BONE MARROW CELLS; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVOUS SYSTEM; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 79959253736     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-2011-0591     Document Type: Article

References (94)

1. Agosti, V., Karur, V., Sathyanarayana, P., Besmer, P.&Wojchowski, D.M. (2009). A KIT juxtamembrane PY567-directed pathway provides nonredundant signals for erythroid progenitor cell development and stress erythropoiesis. Exp Hematol, 37, 159-171.
2. Aster, J.C., Pear, W.S. & Blacklow, S.C. (2008). Notch signaling in leukemia. Annu Rev Pathol, 3, 587-613. (Pubitemid 351488294)
3. Azizi, S.A., Stokes, D., Augelli, B.J., DiGirolamo, C. & Prockop, D.J. (1998). 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, 3908-3913. (Pubitemid 28173227)
4. Banfi, A., Bianchi, G., Notaro, R., Luzzatto, L., Cancedda, R. & Quarto, R. (2002). Replicative aging and gene expression in long-term cultures of human bone marrow stromal cells. Tissue Eng, 8, 901-910. (Pubitemid 35397236)
5. Beissbarth, T. & Speed, T.P. (2004). GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics, 20, 1464-1465. (Pubitemid 38931420)
6. Boiret, N., Rapatel, C., Veyrat-Masson, R., Guillouard, L., Gúerin, J.J., Pigeon, P., Descamps, S., Boisgard, S., Berger, M.G. (2005). Characterization of nonexpanded mesenchymal progenitor cells from normal adult human bone marrow. Exp Hematol, 33(2), 219-225. (Pubitemid 40164904)
7. Bondy, C.A.&Cheng, C.M. (2004). Signaling by insulin-like growth factor 1 in brain. Eur J Pharmacol, 490, 25-31. (Pubitemid 38482159)
8. B¨ottner,M., Krieglstein, K.&Unsicker,K. (2000). The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem, 75, 2227-2240.
9. Brazelton, T.R., Rossi, F.M., Keshet, G.I. & Blau, H.M. (2000). From marrow to brain: expression of neuronal phenotypes in adult mice. Science, 290, 1775-1779. (Pubitemid 32004810)
10. Breen, E.C. (2007). VEGF in biological control. J Cell Biochem, 102, 1358-1367. (Pubitemid 350223939)
11. Br¨oker, L.E., Kruyt, F.A. & Giaccone, G. (2005). Cell death independent of caspases: a review. Clin Cancer Res, 11, 3155-3162. (Pubitemid 40627860)
12. Bunnell, B.A., Ylostalo, J. & Kang, S.K. (2006). Common transcriptional gene profile in neurospheres-derived from pATSCs, pBMSCs, and pNSCs. Biochem Biophys Res Commun, 343, 762-771.
13. Castro, R.F., Jackson, K.A., Goodell, M.A., Robertson, C.S., Liu, H. & Shine, H.D. (2002). Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science, 297, 1299. (Pubitemid 34913161)
14. Chen, J.R., Cheng, G.Y., Sheu, C.C., Tseng, G.F., Wang, T.J. & Huang, Y.S. (2008). Transplanted bone marrow stromal cells migrate, differentiate and improve motor function in rats with experimentally induced cerebral stroke. J Anat, 213, 249-258.
15. Cheng, H.L., Russell, J.W. & Feldman, E.L. (1999). IGF-I promotes peripheral nervous system myelination. Ann N Y Acad Sci, 883, 124-130. (Pubitemid 129495422)
16. Cheng, C.M., Mervis, R.F., Niu, S.L., Salem, N. Jr., Witters, L.A., Tseng, V., Reinhardt, R. & Bondy, C.A. (2003). Insulin-like growth factor 1 is essential for normal dendritic growth. J Neurosci Res, 73, 1-9. (Pubitemid 36791365)
17. Claps, C.M., Corcoran, K.E., Cho, K.J. & Rameshwar, P. (2005). Stromal derived growth factor-1 alpha as a beacon for stem cell homing in development and injury. Curr Neurovasc Res, 2, 319-329. (Pubitemid 41297369)
18. Delaunay, D., Heydon, K., Cumano, A, Schwab, M.H., Thomas, J.L., Suter, U., Nave, K.A., Zalc, B. & Spassky, N. (2008). Early neuronal and glial fate restriction of embryonic neural stem cells. J Neurosci, 28, 2551-2562. (Pubitemid 351348193)
19. Delorme, B. & Chabord, P. (2007). Culture and characterization of human bone marrow mesenchymal stem cells. Meth Mol Med, 140, 67-81.
20. Deng,W., Obrocka, M., Fischer, I., & Prockop, D.J. (2001). 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, 148-152. (Pubitemid 32924357)
21. D¨orr, J., Bechmann, I.,Waiczies, S., Aktas, O.,Walczak, H., Krammer, P.H., Nitsch, R. & Zipp, F. (2002). Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J Neurosci, 22, RC209.
22. Dupont, E., Sansal, I., Evrard, C. & Rouget, P. (1998). Developmental pattern of expression of NPDC-1 and its interaction with E2F-1 suggest a role in the control of proliferation and differentiation of neural cells. J Neurosci Res, 51, 257-267. (Pubitemid 28073033)
23. Elias, L.A., Wang, D.D. & Kriegstein, A.R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature, 448, 901-907. (Pubitemid 47312775)
24. Ernsberger, U. (2008). The role of GDNF family ligand signalling in the differentiation of sympathetic and dorsal root ganglion neurons. Cell Tissue Res, 333, 353-371.
25. Eugenin, E.A., D?Aversa, T.G., Lopez, L., Calderon, T.M. & Berman, J.W. (2003). MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J Neurochem, 85, 1299-1311. (Pubitemid 36613277)
26. Frank, O., Heim, M., Jakob, M., Barbero, A., Schafer, D., Bendik, I., Dick,W., Heberer, M., & Martin, I. (2002). Real-time quantitative RT-PCR analysis of human bone marrow stromal cells during osteogenic differentiation in vitro. J Cell Biochem, 85, 737-746. (Pubitemid 34462784)
27. Franssen, E.H., De Bree, F.M., Essing, A.H., Ramon-Cueto, A. & Verhaagen, J. (2008). Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia, 56, 1285-1298.
28. Garcia, R., Aguiar, J., Alberti, E., de la Cuetara, K. & Pavon, N. (2004). Bone marrow stromal cells produce nerve growth factor and glial cell line-derived neurotrophic factors. Biochem Biophys Res Commun, 316, 753-754. (Pubitemid 38368017)
29. Gilyarov, A.V. (2008). Nestin in central nervous system cells. Neurosci Behav Physiol, 38, 165-169.
30. Haupt, C., Witte, O.W. & Frahm, C. (2007). Up-regulation of Connexin43 in the glial scar following photothrombotic ischemic injury. Mol Cell Neurosci, 35, 89-99. (Pubitemid 46636303)
31. Hermann, A., Maisel, M.&Storch, A. (2006). Epigenetic conversion of human adult bone mesodermal stromal cells into neuroectodermal cell types for replacement therapy of neurodegenerative disorders. Expert Opin Biol Ther, 6, 653-670.
32. Hess, D.C. & Borlongan, C.V. (2008). Cell-based therapy in ischemic stroke. Expert Rev Neurother, 8, 1193-1201.
33. Hofstetter, C.P., Schwarz, E.J., Hess, D., Widenfalk, J., El Manira, A., Prockop, D.J. & Olson, L. (2002). Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A, 99, 2199-2204. (Pubitemid 34169038)
34. Holz, A., Schaeren-Wiemers, N., Schaefer, C., Pott, U., Colello, R.J. & Schwab, M.E. (1999). Molecular and developmental characterization of novel cDNAs of the myelin-associated/ oligodendrocytic basic protein. Cell Res, 9, 179-188.
35. Irvin, D.K., Zurcher, S.D., Nguyen, T.,Weinmaster,G.&Kornblum, H.I. (2001). Expression patterns of Notch1, Notch2, and Notch3 suggest multiple functional roles for the Notch-DSL signaling system during brain development. J Comp Neurol, 436, 167-181. (Pubitemid 32622529)
36. 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., Du, J., Aldrich, S., Lisberg, A., Low, W.C., Largaespada, D.A. & Verfaillie, C.M. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature, 418, 41-49. (Pubitemid 34742565)
37. Jiminez, C.R., Stam, F.J., Li, K.W., Gouwenberg, Y., Hornshaw, M.P., De Winter, F., Verhaagen, J. & Smit, A.B. (2005). Proteomics of the injured rat sciatic nerve reveals protein expression dynamics during regeneration. Mol Cell Proteomics, 4, 120-132. (Pubitemid 40361175)
38. Kageyama, R. & Ohtsuka, T. (1996). The Notch-Hes pathway in mammalian neural development. J Neurosci, 16, 467-477.
39. Kageyama, R., Ohtsuka, T., Shimojo H. & Imayoshi I. (2008). Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat Neurosci, 11, 1247-1251.
40. Kawai, S., Yamauchi, M., Wakisaka, S., Ooshima, T. & Amano, A. (2007). Zinc-finger transcription factor odd-skipped related 2 is one of the regulators in osteoblast proliferation and bone formation. J Bone Miner Res, 22, 1362-1372. (Pubitemid 351339681)
41. Kim, R., Emi, M., Tanabe, K., Murakami, S., Uchida, Y. & Arihiro, K. (2006). Regulation and interplay of apoptotic and nonapoptotic cell death. J Pathol, 208, 319-326. (Pubitemid 43210518)
42. Koelsch, A., Feng, Y., Fink, D.J. & Mata, M. (2010). Transgenemediated GDNF expression enhances synaptic connectivity and GABA transmission to improve functional outcome after spinal cord contusion. J Neurochem, 113(1), 143-152.
43. Koshizuka, S., Okada, S., Okawa, A., Koda, M., Murasawa, M., Hashimoto, M., Kamada, T., Yoshinaga, K., Murakami, M., Moriya, H. & Yamazaki, M. (2004). 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, 64-72. (Pubitemid 38030234)
44. Labouyrie, E., Dubus, P., Groppi, A., Mahon, F.X., Ferrer, J., Parrens, M., Reiffers, J., de Mascarel, A. &Merlio, J.P. (1999). Expression of neurotrophins and their receptors in human bone marrow. Am J Pathol, 154, 405-415. (Pubitemid 29094091)
45. Lee, K.K., Tang, M.K., Yew, D.T., Chow, P.H., Yee, S.P., Schneider, C. & Brancolini, C. (1999). Gas2 is a multifunctional gene involved in the regulation of apoptosis and chondrogenesis in the developing mouse limb. Dev Biol, 207, 14-25. (Pubitemid 29117797)
46. Lee, R.H., Kim, B., Choi, I., Kim, H., Choi, H.S., Suh, K., Bae, Y.C. & Jung, J.S. (2004). Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem, 14, 311-324. (Pubitemid 39179200)
47. Lendahl, U., Zimmerman, L.B. & McKay, R.D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell, 60, 585-595.
48. Li, M. & Ransohoff, R.M. (2008). Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog Neurobiol, 84, 116-131.
49. Liang, G., Cline, G.W. & Macica, C.M. (2007). IGF-1 stimulates de novo fatty acid biosynthesis by Schwann cells during myelination. Glia, 55, 632-641. (Pubitemid 46474304)
50. Lopez-Fanarraga, M., Carranza, G., Bellido, J., Kortazar, D., Villegas, J.C. & Zabala, J.C. (2007). Tubulin cofactor B plays a role in the neuronal growth cone. J Neurochem, 100, 1680-1687. (Pubitemid 46376209)
51. Lu, P., Blesch, A. & Tuszynski, M.H. (2004). Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact? J Neurosci Res, 77, 174-191. (Pubitemid 38859403)
52. Mason, H.A., Rakowiecki, S.M., Raftopoulou, M., Nery, S., Huang, Y., Gridley, T. & Fishell, G. (2005). Notch signaling coordinates the patterning of striatal compartments. Development, 132, 4247-4258. (Pubitemid 41576687)
53. Mecha, M., Rabad́an, M.A., Pẽna-Melían, A., Valencia, M., Mond́ejar, T. & Blanco, M.J. (2008). Expression of TGFbetas in the embryonic nervous system: analysis of interbalance between isoforms. Dev Dyn, 237, 1709-1717. (Pubitemid 351813068)
54. Nandoe Tewarie, R.D., Hurtado, A., Levi, A.D., Grotenhuis, J.A. & Oudega,M. (2006). Bone marrow stromal cells for repair of the spinal cord: towards clinical application. Cell Transplant, 15, 563-577. (Pubitemid 44904669)
55. Nandoe Tewarie, R.D., Hurtado, A., Ritfeld, G.J., Rahiem, S.T., Wendell, D.F., Barroso, M.M., Grotenhuis, J.A., Oudega, M. (2009). Bone marrow stromal cells elicit tissue sparing after acute but not delayed transplantation into the contused adult rat thoracic spinal cord. J Neurotrauma, 26, 2313-2322.
56. Nesbitt, T.L., Roberts, A., Tan, H., Junor, L., Yost, M.J., Potts, J.D., Dettman, R.W. & Goodwin, R.L. (2009). Coronary endothelial proliferation and morphogenesis are regulated by a VEGFmediated pathway. Dev Dyn, 238, 423-430.
57. Neuhuber, B., Gallo, G., Howard, L., Kostura, L., Mackay, A. & Fischer, I. (2004). 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, 192-204. (Pubitemid 38859404)
58. Nissim, S., Hasso, S.M., Fallon, J.F.&Tabin, C.J. (2006). Regulation of Gremlin expression in the posterior limb bud. Dev Biol, 299, 12-21. (Pubitemid 44528396)
59. Mũnoz-Elias, G., Marcus, A.J., Coyne, T.M.,Woodbury,D.&Black, I.B. (2004). Adult bone marrow stromal cells in the embryonic brain: engraftment, migration, differentiation, and long-term survival. J Neurosci, 24, 4585-4595. (Pubitemid 38656614)
60. Ogawa, R. (2006). The importance of adipose-derived stem cells and vascularized tissue regeneration in the field of tissue transplantation. Curr Stem Cell Res Ther, 1, 13-20.
61. Ohshima, Y., Kubo, T., Koyama, R., Ueno, M., Nakagawa, M. & Yamashita, T. (2008). Regulation of axonal elongation and pathfinding from the entorhinal cortex to the dentate gyrus in the hippocampus by the chemokine stromal cell-derived factor 1 alpha. J Neurosci, 28, 8344-8353.
62. Parr, A.M., Tator, C.H. & Keating, A. (2007). Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant, 40, 609-619. (Pubitemid 47456475)
63. Parr, A.M., Kulbatski, I. & Tator, C.H. (2007). Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma, 24, 835-845. (Pubitemid 46799275)
64. Parr, A.M., Kulbatski, I., Zahir, T., Wang, X., Yue, C., Keating, A. & Tator, C.H. (2008). Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience, 155, 760-770.
65. Patten, B.A., Peyrin, J.M., Weinmaster, G. & Corfas, G. (2003). Sequential signaling through Notch1 and erbB receptors mediates radial glia differentiation. J Neurosci, 23, 6132-6140. (Pubitemid 36859451)
66. Ratajczak, M.Z., Luger, S.M. & Gewirtz, A.M. (1992). The c-kit proto-oncogene in normal and malignant human hematopoiesis. Int J Cell Cloning, 10, 205-214.
67. Ritfeld, G.J., Nandoe Tewarie, R.D., Rahiem, S.T., Hurtado, A., Roos, R.A., Grotenhuis, A., Oudega, M. (2010). Reducing macrophages to improve bone marrow stromal cell survival in the contused spinal cord. Neuroreport, 21, 221-226.
68. 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. & Sanberg, P.R. (2000). Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol, 164, 247-256. (Pubitemid 32008970)
69. Sariola, H. & Saarma, M. (2003). Novel functions and signaling pathways for GDNF. J Cell Sci, 116, 3855-3862. (Pubitemid 37279301)
70. Schachner, M. & Bartsch, U. (2000). Multiple functions of the myelin-associated glycoprotein MAG (siglec-4 a) in formation and maintenance of myelin. Glia, 29, 154-165. (Pubitemid 30044510)
71. Schäaffler, A. & Bäuchler, C. (2007). Concise review: adipose tissuederived stromal cells - basic and clinical implications for novel cell-based therapies. Stem Cells, 25, 818-827. (Pubitemid 46572577)
72. Seshi, B., Kumar, S. & King, D. (2003). Multilineage gene expression in human bone marrow stromal cells as evidenced by single-cell microarray analysis. Blood Cells Mol Dis, 31, 268-285.
73. Shannan, B., Seifert, M., Boothman, D.A., Tilgen, W. & Reichrath, J. (2006). Clusterin and DNA repair: a new function in cancer for a key player in apoptosis and cell cycle control. J Mol Histol, 37, 183-188. (Pubitemid 44795623)
74. Smyth, G.K. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol, 3, Article3.
75. Spencer, M.L., Theodosiou, M. & Noonan, D.J. (2004). NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J Biol Chem, 279, 37069-37078. (Pubitemid 39129057)
76. Steiling, H. & Werner, S. (2003). Fibroblast growth factors: key players in epithelial morphogenesis, repair and cytoprotection. Curr Opin Biotechnol, 14, 533-537. (Pubitemid 37298040)
77. Stewart, A.L., Anderson, R.B., Kobayashi, K. & Young, H.M. (2008). Effects of NGF, NT-3 and GDNF family members on neurite outgrowth and migration from pelvic ganglia from embryonic and newborn mice. BMC Dev Biol, 8, 73.
78. Sun, W.W., Zhao, W. & Wang, T.H. (2001). Effects of electroacupuncture onPDGFexpression in spared dorsal root ganglion and associated dorsal horn subjected to partial dorsal root ganglionectomy in cats. Neurochem Res, 33(3), 437-443.
79. Tang,W.,Wang,W., Zhang,Y., Liu, S., Liu, Y. & Zheng, D. (2009). Tumour necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced chemokine release in both TRAIL-resistant and TRAIL-sensitive cells via nuclear factor kappa B. FEBS J, 276, 581-593.
80. Trougakos, I.P., Lourda, M., Agiostratidou, G., Kletsas, D.&Gonos, E.S. (2005). Differential effects of clusterin/apolipoprotein J on cellular growth and survival. Free Radic Biol Med, 38, 436-449. (Pubitemid 40247435)
81. Umemori, H., Linhoff, M.W., Ornitz, D.M. & Sanes, J.R. Cell. (2004). FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell, 118, 257-270. (Pubitemid 38962580)
82. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol, 3(7), RESEARCH0034.
83. Widenfalk, J., Lipson, A., Jubran, M., Hofstetter, C., Ebendal, T., Cao, Y. & Olson, L. (2003). Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience, 120(4), 951-960. (Pubitemid 36966647)
84. Wislet-Gendebien, S., Hans, G., LePrince, P., Rigo, J.M., Moonen, G. & Rogister, B. (2005). Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells, 23, 392-402. (Pubitemid 40404458)
85. Yaghoobi, M.M.&Mowla, S.J. (2006). Differential gene expression pattern of neurotrophins and their receptors during neuronal differentiation of rat bone marrow stromal cells. Neurosci Lett, 397, 149-154. (Pubitemid 43340477)
86. Yaghoobi, M.M. & Mahani, M.T. (2008). NGF and BDNF expression drop off in neurally differentiated bone marrow stromal stem cells. Brain Res, 1203, 26-31.
87. Yakovlev, A.G. & Faden, A.I. (2004). Mechanisms of neural cell death: implications for development of neuroprotective treatment strategies. NeuroRx, 1, 5-16. (Pubitemid 46589338)
88. Yamagata, K., Sanders, L.K., Kaufmann, W.E., Yee, W., Barnes, C.A., Nathans, D. & Worley, P.F. (1994). Rheb, a growth factor- and synaptic activity-regulated gene, encodes a novel Ras-related protein. J Biol Chem, 269, 16333-16339. (Pubitemid 24209331)
89. Ye, M., Chen, S.,Wang, X., Qi, C., Lu, G., Liang, L.&Xu, J. (2005). Glial cell line-derived neurotrophic factor in bone marrow stromal cells of rat. Neurorep, 16, 581-585.
90. Yokoyama, A., Sakamoto, A., Kameda, K., Imai, Y. & Tanaka, J. (2006). NG2 proteoglycan-expressing microglia as multipotent neural progenitors in normal and pathologic brains. Glia, 53, 754-768.
91. Yoo, S. & Wrathall, J.R. (2007). Mixed primary culture and clonal analysis provide evidence that NG2 proteoglycan-expressing cells after spinal cord injury are glial progenitors. Dev Neurobiol, 67, 860-874. (Pubitemid 47066917)
92. Zhang, W., Bae, I., Krishnaraju, K., Azam, N., Fan, W., Smith, K., Hoffman, B.&Liebermann, D.A. (1999). CR6:Athird member in the MyD118 and Gadd45 gene family which functions in negative growth control. Oncogene, 18, 4899-4907. (Pubitemid 29425296)
93. Zurita, M. & Vaquero, J. (2004). Functional recovery in chronic paraplegia after bone marrow stromal cells transplantation. Neurorep, 15, 1105-1108. (Pubitemid 38670061)
94. Zuzarte-Luis, V., Montero, J.A., Kawakami, Y., Izpisua-Belmonte, J.C. & Hurle, J.M. (2007). Lysosomal cathepsins in embryonic programmed cell death. Dev Biol, 301, 205-217. (Pubitemid 44958390)