Adult neural stem cells: Response to stroke injury and potential for therapeutic applications

Current Stem Cell Research and Therapy

Volumn 6, Issue 4, 2011, Pages 327-338

  Barkho, Basam Z ^a,b   Zhao, Xinyu ^a,c  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Adult neurogenesis; Neural stem progenitor cells; Stem cell niche; Stem cell therapy; Stroke; Stroke induced neuro genesis

Indexed keywords

ARTICLE; BRAIN INJURY; CELL CONTACT; CELL DIFFERENTIATION; CELL MIGRATION; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STROKE;

EID: 80055106822     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488811797904362     Document Type: Article

References (150)

1. Doetsch F. The glial identity of neural stem cells. Nat Neurosci 2003; 6: 1127-34.
2. Duan X, Kang E, Liu CY, Ming GL, Song H. Development of neural stem cell in the adult brain. Curr Opin Neurobiol 2008; 18: 108-15.
3. Lie DC, Song H, Colamarino SA, Ming GL, Gage FH. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 2004; 44: 399-421.
4. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002; 415: 1030-4.
5. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008; 132: 645-60.
6. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005; 28: 223-50.
7. Kee N, Teixeira CM, Wang AH, Frankland PW. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 2007; 10: 355-62.
8. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997; 17: 5046-61.
9. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2001; 2: 287-93.
10. Ma DK, Bonaguidi MA, Ming GL, Song H. Adult neural stem cells in the mammalian central nervous system. Cell Res 2009; 19: 672-82.
11. Doetsch F, Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 1996; 93: 14895-900.
12. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996; 271: 978-81.
13. Rochefort C, Gheusi G, Vincent JD, Lledo PM. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 2002; 22: 2679-89.
14. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009; 32: 149-84.
15. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004; 101: 17528-32.
16. Gage FH. Mammalian neural stem cells. Science 2000; 287: 1433-8.
17. Horner PJ, Gage FH. Regenerating the damaged central nervous system. Nature 2000; 407: 963-70.
18. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature 2000; 405: 951-5.
19. Nakatomi H, Kuriu T, Okabe S, et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 2002; 110: 429-41.
20. Kolb B, Morshead C, Gonzalez C, et al. Growth factor-stimulated generation of new cortical tissue and functional recovery after stroke damage to the motor cortex of rats. J Cereb Blood Flow Metab 2007; 27: 983-97.
21. Prevention CoDCCa. Prevalence of disabilities and associated health conditions among adults--United States, 1999. MMWR Morb Mortal Wkly Rep 2001; 50: 120-5.
22. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 1999; 22: 391-7.
23. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003; 4: 399-415.
24. Tsuchihashi Y, Kitamura T, Fujita S. Immunofluorescence studies of the monocytes in the injured rat brain. Acta Neuropathol 1981; 53: 213-9.
25. Giulian D, Chen J, Ingeman JE, George JK, Noponen M. The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J Neurosci 1989; 9: 4416-29.
26. del Zoppo GJ, Milner R, Mabuchi T, et al. Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke 2007; 38: 646-51.
27. Barone FC, Feuerstein GZ. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999; 19: 819-34.
28. Feuerstein G, Wang X, Barone FC. Cytokines in brain ischemia the role of TNF alpha. Cell Mol Neurobiol 1998; 18: 695-701.
29. Pober JS, Cotran RS. Cytokines and endothelial cell biology. Physiol Rev 1990; 70: 427-51.
30. Suzuki Y, Nagai N, Yamakawa K, Kawakami J, Lijnen HR, Umemura K. Tissue-type plasminogen activator (t-PA) induces stromelysin-1 (MMP-3) in endothelial cells through activation of lipoprotein receptor-related protein. Blood 2009; 114: 3352-8.
31. Sumii T, Lo EH. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 2002; 33: 831-6.
32. Adibhatla RM, Hatcher JF. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol Disord Drug Targets 2008; 7: 243-53.
33. Kilic E, Bahr M, Hermann DM. Effects of recombinant tissue plasminogen activator after intraluminal thread occlusion in mice: role of hemodynamic alterations. Stroke 2001; 32: 2641-7.
34. Kernie SG, Parent JM. Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol Dis 2010; 37: 267-74.
35. Parent JM, Valentin VV, Lowenstein DH. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci 2002; 22: 3174-88.
36. Kokaia Z, Lindvall O. Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 2003; 13: 127-32.
37. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 2004; 10 Suppl: S42-S50.
38. Jin K, Sun Y, Xie L, et al. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 2003; 24: 171-89.
39. Kuge A, Takemura S, Kokubo Y, Sato S, Goto K, Kayama T. Temporal profile of neurogenesis in the subventricular zone, dentate gyrus and cerebral cortex following transient focal cerebral ischemia. Neurol Res 2009; 31: 969-76.
40. Zhang RL, Zhang ZG, Zhang L, Chopp M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 2001; 105: 33-41.
41. Takasawa K, Kitagawa K, Yagita Y, et al. Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 2002; 22: 299-307.
42. Tonchev AB, Yamashima T, Sawamoto K, Okano H. Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia. J Neurosci Res 2005; 81: 776-88.
43. Lichtenwalner RJ, Parent JM. Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 2006; 26: 1-20.
44. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8: 963-70.
45. Barkho B, Zhao X. Neural stem cell migration: Roles of chemokines and proteases. In Jin K, Ed. Adult Neurogenesis and Central Nervous System Diseases; Research Signpost 2010; pp. 65-90.
46. Goings GE, Sahni V, Szele FG. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res 2004; 996: 213-26.
47. Hagberg H, Mallard C. Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 2005; 18: 117-23.
48. Das S, Basu A. Inflammation: a new candidate in modulating adult neurogenesis. J Neurosci Res 2008; 86: 1199-208.
49. Vitkovic L, Bockaert J, Jacque C. Inflammatory cytokines: neuromodulators in normal brain? J Neurochem 2000; 74: 457-71.
50. Laing KJ, Secombes CJ. Chemokines. Dev Comp Immunol 2004; 28: 443-60.
51. Laing KJ, Secombes CJ. Trout CC chemokines: comparison of their sequences and expression patterns. Mol Immunol 2004; 41: 793-808.
52. Asensio VC, Campbell IL. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci 1999; 22: 504-12.
53. Kokovay E, Goderie S, Wang Y, et al. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 2010; 7: 163-73.
54. Thored P, Arvidsson A, Cacci E, et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 2006; 24: 739-47.
55. Zhang ZG, Zhang L, Tsang W, et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002; 22: 379-92.
56. Wiltrout C, Lang B, Yan Y, Dempsey RJ, Vemuganti R. Repairing brain after stroke: a review on post-ischemic neurogenesis. Neurochem Int 2007; 50: 1028-41.
57. Tran PB, Ren D, Veldhouse TJ, Miller RJ. Chemokine receptors are expressed widely by embryonic and adult neural progenitor cells. J Neurosci Res 2004; 76: 20-34.
58. Barkho BZ, Munoz AE, Li X, Li L, Cunningham LA, Zhao X. Endogenous Matrix Metalloproteinase (MMP)-3 and MMP-9 Promote the Differentiation and Migration of Adult Neural Progenitor Cells in Response to Chemokines. Stem Cells 2008; 26(12): 3139-49.
59. Kim JS. Cytokines and adhesion molecules in stroke and related diseases. J Neurol Sci 1996; 137: 69-78.
60. Otto VI, Gloor SM, Frentzel S, et al. The production of macrophage inflammatory protein-2 induced by soluble intercellular adhesion molecule-1 in mouse astrocytes is mediated by src tyrosine kinases and p42/44 mitogen-activated protein kinase. J Neurochem 2002; 80: 824-34.
61. Hallbergson AF, Gnatenco C, Peterson DA. Neurogenesis and brain injury: managing a renewable resource for repair. J Clin Invest 2003; 112: 1128-33.
62. Venstrom KA, Reichardt LF. Extracellular matrix. 2: Role of extracellular matrix molecules and their receptors in the nervous system. Faseb J 1993; 7: 996-1003.
63. Takada Y, Kamata T, Irie A, Puzon-McLaughlin W, Zhang XP. Structural basis of integrin-mediated signal transduction. Matrix Biol 1997; 16: 143-51.
64. Schmid RS, Anton ES. Role of integrins in the development of the cerebral cortex. Cereb Cortex 2003; 13: 219-24.
65. Ohab JJ, Fleming S, Blesch A, Carmichael ST. A neurovascular niche for neurogenesis after stroke. J Neurosci 2006; 26: 13007-16.
66. Wang L, Zhang ZG, Zhang RL, et al. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 2006; 26: 5996-6003.
67. Lee SR, Kim HY, Rogowska J, et al. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 2006; 26: 3491-5.
68. Belvindrah R, Hankel S, Walker J, Patton BL, Muller U. Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci 2007; 27: 2704-17.
69. Kearns SM, Laywell ED, Kukekov VK, Steindler DA. Extracellular matrix effects on neurosphere cell motility. Exp Neurol 2003; 182: 240-4.
70. Pufe T, Harde V, Petersen W, Goldring MB, Tillmann B, Mentlein R. Vascular endothelial growth factor (VEGF) induces matrix metalloproteinase expression in immortalized chondrocytes. J Pathol 2004; 202: 367-74.
71. Seiki M. The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr Opin Cell Biol 2002; 14: 624-32.
72. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 2003; 200: 448-64.
73. Chang C, Werb Z. The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 2001; 11: S37-43.
74. Mannello F, Tonti GA, Bagnara GP, Papa S. Role and function of matrix metalloproteinases in the differentiation and biological characterization of mesenchymal stem cells. Stem Cells 2006; 24: 475-81.
75. Cunningham LA, Wetzel M, Rosenberg GA. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 2005; 50: 329-39.
76. Bovetti S, Bovolin P, Perroteau I, Puche AC. Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodelling. Eur J Neurosci 2007; 25: 2021-33.
77. Streuli C. Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol 1999; 11: 634-40.
78. Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 2005; 21: 605-31.
79. Doetsch F. A niche for adult neural stem cells. Curr Opin Genet Dev 2003; 13: 543-50.
80. Giaume C, Venance L. Gap junctions in brain glial cells and development. Perspect Dev Neurobiol 1995; 2: 335-45.
81. Dermietzel R, Spray DC. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 1993; 16: 186-92.
82. Duval N, Gomes D, Calaora V, Calabrese A, Meda P, Bruzzone R. Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells. J Cell Sci 2002; 115: 3241-51.
83. Rozental R, Morales M, Mehler MF, et al. Changes in the properties of gap junctions during neuronal differentiation of hippocampal progenitor cells. J Neurosci 1998; 18: 1753-62.
84. Kunze A, Congreso MR, Hartmann C, et al. Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 2009; 106: 11336-41.
85. Huang GY, Cooper ES, Waldo K, Kirby ML, Gilula NB, Lo CW. Gap junction-mediated cell-cell communication modulates mouse neural crest migration. J Cell Biol 1998; 143: 1725-34.
86. Huber AH, Weis WI. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 2001; 105: 391-402.
87. Shapiro L. Beta-catenin and its multiple partners: promiscuity explained. Nat Struct Biol 2001; 8: 484-487.
88. Lobo MV, Alonso FJ, Redondo C, et al. Cellular characterization of epidermal growth factor-expanded free-floating neurospheres. J Histochem Cytochem 2003; 51: 89-103.
89. Seki T, Namba T, Mochizuki H, Onodera M. Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 2007; 502: 275-90.
90. Little L, Healy KE, Schaffer D. Engineering biomaterials for synthetic neural stem cell microenvironments. Chem Rev 2008; 108: 1787-96.
91. Saha K, Pollock JF, Schaffer DV, Healy KE. Designing synthetic materials to control stem cell phenotype. Curr Opin Chem Biol 2007; 11: 381-7.
92. Robertson MJ, Gip P, Schaffer DV. Neural stem cell engineering: directed differentiation of adult and embryonic stem cells into neurons. Front Biosci 2008; 13: 21-50.
93. Rossi F, Cattaneo E. Opinion: neural stem cell therapy for neurological diseases: dreams and reality. Nat Rev Neurosci 2002; 3: 401-9.
94. Freed CR, Greene PE, Breeze RE, et al. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 2001; 344: 710-9.
95. Katakowski M, Chen J, Zhang ZG, Santra M, Wang Y, Chopp M. Stroke-induced subventricular zone proliferation is promoted by tumor necrosis factor-alpha-converting enzyme protease activity. J Cereb Blood Flow Metab 2007; 27: 669-78.
96. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 2002; 52: 802-13.
97. Haas S, Weidner N, Winkler J. Adult stem cell therapy in stroke. Curr Opin Neurol 2005; 18: 59-64.
98. Benraiss A, Chmielnicki E, Lerner K, Roh D, Goldman SA. Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 2001; 21: 6718-31.
99. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 2002; 99: 11946-50.
100. Cairns K, Finklestein SP. Growth factors and stem cells as treatments for stroke recovery. Phys Med Rehabil Clin N Am 2003; 14: S135-42.
101. Toth ZE, Leker RR, Shahar T, et al. The combination of granulocyte colony-stimulating factor and stem cell factor significantly increases the number of bone marrow-derived endothelial cells in brains of mice following cerebral ischemia. Blood 2008; 111: 5544-52.
102. Marti HJ, Bernaudin M, Bellail A, et al. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 2000; 156: 965-76.
103. Hayashi T, Watabe H, Kudomi N, et al. A theoretical model of oxygen delivery and metabolism for physiologic interpretation of quantitative cerebral blood flow and metabolic rate of oxygen. J Cereb Blood Flow Metab 2003; 23: 1314-23.
104. Zhang ZG, Zhang L, Jiang Q, et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 2000; 106: 829-38.
105. Wang L, Zhang Z, Wang Y, Zhang R, Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004; 35: 1732-7.
106. Arai K, Jin G, Navaratna D, Lo EH. Brain angiogenesis in developmental and pathological processes: neurovascular injury and angiogenic recovery after stroke. FEBS J 2009; 276: 4644-52.
107. Chopp M, Zhang ZG, Jiang Q. Neurogenesis, angiogenesis, and MRI indices of functional recovery from stroke. Stroke 2007; 38: 827-31.
108. Goh EL, Ma D, Ming GL, Song H. Adult neural stem cells and repair of the adult central nervous system. J Hematother Stem Cell Res 2003; 12: 671-9.
109. Morrison SJ. Stem cell potential: can anything make anything? Curr Biol 2001; 11: R7-9.
110. Anderson DJ, Gage FH, Weissman IL. Can stem cells cross lineage boundaries? Nat Med 2001; 7: 393-5.
111. Lindvall O. Clinical application of neuronal grafts in Parkinson's disease. J Neurol 1994; 242: S54-6.
112. Fisher LJ, Gage FH. Intracerebral transplantation: basic and clinical applications to the neostriatum. FASEB J 1994; 8: 489-96.
113. Langston JW. The promise of stem cells in Parkinson disease. J Clin Invest 2005; 115: 23-5.
114. Srivastava AS, Malhotra R, Sharp J, Berggren T. Potentials of ES cell therapy in neurodegenerative diseases. Curr Pharm Des 2008; 14: 3873-9.
115. Menendez P, Wang L, Bhatia M. Genetic manipulation of human embryonic stem cells: a system to study early human development and potential therapeutic applications. Curr Gene Ther 2005; 5: 375-85.
116. Shufaro Y, Reubinoff BE. Therapeutic applications of embryonic stem cells. Best Pract Res Clin Obstet Gynaecol 2004; 18: 909-27.
117. Martino G, Pluchino S. The therapeutic potential of neural stem cells. Nat Rev Neurosci 2006; 7: 395-406.
118. Osakada F, Ikeda H, Sasai Y, Takahashi M. Stepwise differentiation of pluripotent stem cells into retinal cells. Nat Protoc 2009; 4: 811-24.
119. Idelson M, Alper R, Obolensky A, et al. Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 2009; 5: 396-408.
120. Lu B, Malcuit C, Wang S, et al. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 2009; 27: 2126-35.
121. Garber K. Biotech in a blink. Nat Biotechnol 2010; 28: 311-4.
122. Yamanaka S, Blau HM. Nuclear reprogramming to a pluripotent state by three approaches. Nature 2010; 465: 704-12.
123. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-76.
124. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-20.
125. Muller T, Fleischmann G, Eildermann K, et al. A novel embryonic stem cell line derived from the common marmoset monkey (Callithrix jacchus) exhibiting germ cell-like characteristics. Hum Reprod 2009; 24: 1359-72.
126. Lyssiotis CA, Foreman RK, Staerk J, et al. Reprogramming of murine fibroblasts to induced pluripotent stem cells with chemical complementation of Klf4. Proc Natl Acad Sci USA 2009; 106: 8912-7.
127. Huangfu D, Osafune K, Maehr R, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008; 26: 1269-75.
128. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008; 321: 1218-21.
129. Skyler JS. Cellular therapy for type 1 diabetes: has the time come? Jama 2007; 297: 1599-600.
130. Seldin DC, Anderson JJ, Skinner M, et al. Successful treatment of AL amyloidosis with high-dose melphalan and autologous stem cell transplantation in patients over age 65. Blood 2006; 108: 3945-7.
131. Childs R, Chernoff A, Contentin N, et al. Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation. N Engl J Med 2000; 343: 750-8.
132. Taguchi A, Soma T, Tanaka H, et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 2004; 114: 330-8.
133. Peterson DA. Umbilical cord blood cells and brain stroke injury: bringing in fresh blood to address an old problem. J Clin Invest 2004; 114: 312-4.
134. Haylock DN, Nilsson SK. Expansion of umbilical cord blood for clinical transplantation. Curr Stem Cell Res Ther 2007; 2: 324-35.
135. Ballen KK. New trends in umbilical cord blood transplantation. Blood 2005; 105: 3786-92.
136. Ballen KK. Advances in umbilical cord blood transplantation. Curr Stem Cell Res Ther 2006; 1: 317-24.
137. Liao W, Xie J, Zhong J, et al. Therapeutic effect of human umbilical cord multipotent mesenchymal stromal cells in a rat model of stroke. Transplantation 2009; 87: 350-9.
138. Bieback K, Kluter H. Mesenchymal stromal cells from umbilical cord blood. Curr Stem Cell Res Ther 2007; 2: 310-23.
139. Coyne TM, Marcus AJ, Woodbury D, Black IB. Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. Stem Cells 2006; 24: 2483-92.
140. Cho GW, Koh SH, Kim MH, et al. The neuroprotective effect of erythropoietin-transduced human mesenchymal stromal cells in an animal model of ischemic stroke. Brain Res 2010; 1353: 1-13.
141. Aoki H, Onodera H, Yae T, Jian Z, Kogure K. Neural grafting to ischemic CA1 lesions in the rat hippocampus: an autoradiographic study. Neuroscience 1993; 56: 345-54.
142. Farber SD, Onifer SM, Kaseda Y, et al. Neural transplantation of horseradish peroxidase-labeled hippocampal cell suspensions in an experimental model of cerebral ischemia. Prog Brain Res 1988; 78: 103-7.
143. Kelly S, Bliss TM, Shah AK, et al. Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci USA 2004; 101: 11839-44.
144. Zhang ZG, Jiang Q, Zhang R, et al. Magnetic resonance imaging and neurosphere therapy of stroke in rat. Ann Neurol 2003; 53: 259-63.
145. Wennersten A, Meier X, Holmin S, Wahlberg L, Mathiesen T. Proliferation, migration, and differentiation of human neural stem/progenitor cells after transplantation into a rat model of traumatic brain injury. J Neurosurg 2004; 100: 88-96.
146. Olstorn H, Moe MC, Roste GK, Bueters T, Langmoen IA. Transplantation of stem cells from the adult human brain to the adult rat brain. Neurosurgery 2007; 60: 1089-98; discussion 98-9.
147. Jeong SW, Chu K, Jung KH, Kim SU, Kim M, Roh JK. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 2003; 34: 2258-63.
148. Takeuchi H, Natsume A, Wakabayashi T, et al. Intravenously transplanted human neural stem cells migrate to the injured spinal cord in adult mice in an SDF-1- and HGF-dependent manner. Neurosci Lett 2007; 426: 69-74.
149. Lee ST, Chu K, Park JE, et al. Intravenous administration of human neural stem cells induces functional recovery in Huntington's disease rat model. Neurosci Res 2005; 52: 243-9.
150. Le Belle JE, Svendsen CN. Stem cells for neurodegenerative disorders: where can we go from here? BioDrugs 2002; 16: 389-401.