Inflammation and stem cell migration to the injured brain in higher organisms

Stem Cells and Development

Volumn 18, Issue 5, 2009, Pages 693-701

  Park, Dong Hyuk ^a,b   Eve, David J ^a   Musso, James ^a   Klasko, Stephen K ^a   Cruz, Eduardo ^c   Borlongan, Cesario V ^a   Sanberg, Paul R ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b Korea University Ansan Hospital   (South Korea)

^c Cryopraxis   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

MACROPHAGE INFLAMMATORY PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN; STROMAL CELL DERIVED FACTOR 1;

BRAIN INJURY; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; INFLAMMATION; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION;

ANIMALS; BRAIN INJURIES; CELL MOVEMENT; HUMANS; INFLAMMATION; MICROGLIA; STEM CELL TRANSPLANTATION; STEM CELLS;

ANIMALIA;

EID: 66249122757     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0008     Document Type: Review

References (105)

1. Hunt DP, KA Irvine, DJ Webber, DA Compston, WF Blakemore and S Chandran. (2008). Effects of direct transplantation of multipotent mesenchymal stromal/stem cells into the demy-elinated spinal cord. Cell Transplant 17:865-873.
2. Jain M, RJ Armstrong, S Elneil and RA Barker. (2006). Transplanted human neural precursor cells migrate widely but show no lesion-specif c tropism in the 6-hydroxydopamine rat model of Parkinson's disease. Cell Transplant 15:579-593.
3. Master Z, M McLeod and I Mendez. (2007). Benef ts, risks and ethical considerations in translation of stem cell research to clinical applications in Parkinson's disease. J Med Ethics 33:169-173.
4. Newman MB, I Misiuta, AE Willing, T Zigova, RC Karl, CV Borlongan and PR Sanberg. (2005). Tumorigenicity issues of embryonic carcinoma-derived stem cells: relevance to surgical trials using NT2 and hNT neural cells. Stem Cells Dev 14:29-43.
5. Wu J, Z Sun, HS Sun, J Wu, RD Weisel, A Keating, ZH Li, ZP Feng and RK Li. (2007). Intravenously administered bone marrow cells migrate to damaged brain tissue and improve neural function in ischemic rats. Cell Transplant 16:993-1005.
6. Kim D, BG Chun, YK Kim, YH Lee, CS Park, I Jeon, C Cheong, TS Hwang, H Chung, BJ Gwag, KS Hong and J Song. (2007). In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant 16:1007-1012.
7. Callera F and CM de Melo. (2007). Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells' migration into the injured site. Stem Cells Dev 16:461-466.
8. Anderson L and MA Caldwell. (2007). Human neural progenitor cell transplants into the subthalamic nucleus lead to functional recovery in a rat model of Parkinson's disease. Neurobiol Dis 27:133-140.
9. Burnstein RM, T Foltynie, X He, DK Menon, CN Svendsen and MA Caldwell. (2004). Differentiation and migration of long term expanded human neural progenitors in a partial lesion model of Parkinson's disease. Int J Biochem Cell Biol 36:702-713.
10. Li XK, AC Guo and PP Zuo. (2003). Survival and differentiation of transplanted neural stem cells in mice brain with MPTP-induced Parkinson disease. Acta Pharmacol Sin 24:1192-1198.
11. Takagi Y, J Takahashi, H Saiki, A Morizane, T Hayashi, Y Kishi, H Fukuda, Y Okamoto, M Koyanagi, M Ideguchi, H Hayashi, T Imazato, H Kawasaki, H Suemori, S Omachi, H Iida, N Itoh, N Nakatsuji, Y Sasai and N Hashimoto. (2005). Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115:102-109.
12. Bjugstad KB, YD Teng, DE Redmond Jr, JD Elsworth, RH Roth, SK Cornelius, EY Snyder and JR Sladek Jr. (2008). Human neural stem cells migrate along the nigrostriatal pathway in a primate model of Parkinson's disease. Exp Neurol 211:362-369.
13. Coyne TM, AJ Marcus, D Woodbury and IB Black. (2006). 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 24:2483-2492.
14. Schafer R, M Ayturan, R Bantleon, R Kehlbach, G Siegel, J Pintaske, S Conrad, H Wolburg, H Northoff, J Wiskirchen and R Weissert. (2008). The use of clinically approved small particles of iron oxide (SPIO) for labeling of mesenchymal stem cells aggravates clinical symptoms in experimental autoimmune encephalomyelitis and influences their in vivo distribution. Cell Transplant 17:923 -941.
15. Bagga V, SB Dunnett and RA Fricker-Gates. (2008). Ascorbic acid increases the number of dopamine neurons in vitro and in transplants to the 6-OHDA-lesioned rat brain. Cell Transplant 17:763-773.
16. Sladek JR Jr, KB Bjugstad, TJ Collier, EA Bundock, BC Blanchard, JD Elsworth, RH Roth and DE Redmond Jr. (2008). Embryonic substantia nigra grafts show directional outgrowth to cografted striatal grafts and potential for pathway reconstruction in nonhuman primate. Cell Transplant 17:427-444.
17. Jiang L, M Newman, S Saporta, N Chen, C Sanberg, PR Sanberg and AE Willing. (2008). MIP-1alpha and MCP-1 induce migration of human umbilical cord blood cells in models of stroke. Curr Neurovasc Res 5:118-124.
18. Newman MB, AE Willing, JJ Manresa, C Davis-Sanberg and PR Sanberg. (2005). Stroke-induced migration of human umbilical cord blood cells: time course and cytokines. Stem Cells Dev 14:576 - 586.
19. Imitola J, K Raddassi, KI Park, FJ Mueller, M Nieto, YD Teng, D Frenkel, J Li, RL Sidman, CA Walsh, EY Snyder and SJ Khoury. (2004). Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/ CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 101:18117-18122.
20. Ozaki Y, M Nishimura, K Sekiya, F Suehiro, M Kanawa, H Nikawa, T Hamada and Y Kato. (2007). Comprehensive analysis of chemotactic factors for bone marrow mesenchymal stem cells. Stem Cells Dev 16:119-129.
21. Schinkothe T, W Bloch and A Schmidt. (2008). In vitro secreting prof le of human mesenchymal stem cells. Stem Cells Dev 17:199-206.
22. Takeuchi H, A Natsume, T Wakabayashi, C Aoshima, S Shimato, M Ito, J Ishii, Y Maeda, M Hara, SU Kim and J Yoshida. (2007). 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 426:69-74.
23. Shyu WC, SZ Lin, PS Yen, CY Su, DC Chen, HJ Wang and H Li. (2008). Stromal cell-derived factor-1 alpha promotes neuroprotection, angiogenesis, and mobilization/homing of bone marrow-derived cells in stroke rats. J Pharmacol Exp Ther 324:834-849.
24. Wang Y, Y Deng and GQ Zhou. (2008). SDF-1alpha/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res 1195:104-112.
25. Unzek S, M Zhang, N Mal, WR Mills, KR Laurita and MS Penn. (2007). SDF-1 recruits cardiac stem cell-like cells that depolarize in vivo. Cell Transplant 16:879-886.
26. Liapi A, J Pritchett, O Jones, N Fujii, JG Parnavelas and B Nadarajah. (2008). Stromal-derived factor 1 signaling regulates radial and tangential migration in the developing cerebral cortex. Dev Neurosci 30:117-131.
27. Miller RJ, G Banisadr and BJ Bhattacharyya. (2008). CXCR4 signaling in the regulation of stem cell migration and development. J Neuroimmunol 198:31-38.
28. Shen LH, Y Li, J Chen, A Zacharek, Q Gao, A Kapke, M Lu, K Raginski, P Vanguri, A Smith and M Chopp. (2007). Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 27:6-13.
29. Chavakis E, G Carmona, C Urbich, S Gottig, R Henschler, JM Penninger, AM Zeiher, T Chavakis and S Dimmeler. (2008). Phosphatidylinositol-3-kinase-gamma is integral to homing functions of progenitor cells. Circ Res 102:942-949.
30. Zheng H, G Fu, T Dai and H Huang. (2007). Migration of endothelial progenitor cells mediated by stromal cell-derived factor-1alpha/CXCR4 via PI3K/Akt/eNOS signal transduction pathway. J Cardiovasc Pharmacol 50:274-280.
31. Newman MB, AE Willing, JJ Manresa, CD Sanberg and PR Sanberg. (2006). Cytokines produced by cultured human umbilical cord blood (HUCB) cells: implications for brain repair. Exp Neurol 199:201-208.
32. Rogers J, D Mastroeni, B Leonard, J Joyce and A Grover. (2007). Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int Rev Neurobiol 82:235-246.
33. Imamura K, N Hishikawa, M Sawada, T Nagatsu, M Yoshida and Y Hashizume. (2003). Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol 106:518-526.
34. Wilms H, L Zecca, P Rosenstiel, J Sievers, G Deuschl and R Lucius. (2007). Inflammation in Parkinson's diseases and other neurodegenerative diseases: cause and therapeutic implications. Curr Pharm Des 13:1925-1928.
35. Block ML and JS Hong. (2007). Chronic microglial activation and progressive dopaminergic neurotoxicity. Biochem Soc Trans 35:1127-1132.
36. Mosley RL, EJ Benner, I Kadiu, M Thomas, MD Boska, K Hasan, C Laurie and HE Gendelman. (2006). Neuroinflammation, oxi-dative stress and the pathogenesis of Parkinson's Disease. Clin Neurosci Res 6:261-281.
37. Cicchetti F, AL Brownell, K Williams, YI Chen, E Livni and O Isacson. (2002). Neuroinf ammation of the nigrostriatal pathway during progressive 6-OHDA dopamine degeneration in rats monitored by immunohistochemistry and PET imaging. Eur J Neurosci 15:991-998.
38. Yasuda Y, R Shinagawa, M Yamada, T Mori, N Tateishi and S Fujita. (2007). Long-lasting reactive changes observed in micro-glia in the striatal and substantia nigral of mice after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Brain Res 1138:196-202.
39. Leung BK, R Biran, CJ Underwood and PA Tresco. (2008). Characterization of microglial attachment and cytokine release on biomaterials of differing surface chemistry. Biomaterials 29:3289-3297.
40. Belmadani A, PB Tran, D Ren and RJ Miller. (2006). Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 26:3182-3191.
41. Widera D, W Holtkamp, F Entschladen, B Niggemann, K Zanker, B Kaltschmidt and C Kaltschmidt. (2004). MCP-1 induces migration of adult neural stem cells. Eur J Cell Biol 83:381-387.
42. Xu Q, S Wang, X Jiang, Y Zhao, M Gao, Y Zhang, X Wang, K Tano, M Kanehara, W Zhang and T Ishida. (2007). Hypoxia-induced astrocytes promote the migration of neural progenitor cells via vascular endothelial factor, stem cell factor, stromal-derived factor-1alpha and monocyte chemoattractant protein-1 upregulation in vitro. Clin Exp Pharmacol Physiol 34:624-631.
43. Behrstock S, AD Ebert, S Klein, M Schmitt, JM Moore and CN Svendsen. (2008). Lesion-induced increase in survival and migration of human neural progenitor cells releasing GDNF. Cell Transplant 17:753-762.
44. Lu SY, MT Shipley, AB Norman and PR Sanberg. (1991). Striatal, ventral mesencephalic and cortical transplants into the intact rat striatum: a neuroanatomical study. Exp Neurol 113:109 -130.
45. Nishino H, H Hida, N Takei, M Kumazaki, K Nakajima and H Baba. (2000). Mesencephalic neural stem (progenitor) cells develop to dopaminergic neurons more strongly in dop-amine-depleted striatum than in intact striatum. Exp Neurol 16 4: 2 0 9 -214.
46. Walczak P, N Chen, D Eve, J Hudson, T Zigova, J Sanchez-Ramos, PR Sanberg, CD Sanberg and AE Willing. (2007). Long-term cultured human umbilical cord neural-like cells transplanted into the striatum of NOD SCID mice. Brain Res Bull 74:155-163.
47. Del Guerra S, R Giannarelli, M Carmellini, A Coppelli, R Lupi, C Tellini, R Solari, L Meacci, M Calabrese, P Viacava, F Mosca, R Navalesi and P Marchetti. (1997). Bovine-to-porcine intra-thymic islet xenotransplantation. Transplant Proc 29:2061.
48. Nishino H and CV Borlongan. (2000). Restoration of function by neural transplantation in the ischemic brain. Prog Brain Res 127:461-476.
49. Guzman R, T Bliss, A De Los Angeles, M Moseley, T Palmer and G Steinberg. (2008). Neural progenitor cells transplanted into the uninjured brain undergo targeted migration after stroke onset. J Neurosci Res 86:873-882.
50. Wang X, Y Lu, H Zhang, K Wang, Q He, Y Wang, X Liu, L Li and X Wang. (2004). Distinct eff cacy of pre-differentiated versus intact fetal mesencephalon-derived human neural progenitor cells in alleviating rat model of Parkinson's disease. Int J Dev Neurosci 22:175-183.
51. Yan J, AM Welsh, SH Bora, EY Snyder and VE Koliatsos. (2004). Differentiation and tropic/trophic effects of exogenous neural precursors in the adult spinal cord. J Comp Neurol 480:101-114.
52. Yang M, AE Donaldson, CE Marshall, J Shen and L Iacovitti. (2004). Studies on the differentiation of dopaminergic traits in human neural progenitor cells in vitro and in vivo. Cell Transplant 13:535 - 547.
53. Sun L, J Lee and HA Fine. (2004). Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury. J Clin Invest 113:1364-1374.
54. Toth ZE, RR Leker, T Shahar, S Pastorino, I Szalayova, B Asemenew, S Key, A Parmelee, B Mayer, K Nemeth, A Bratincsak and E Mezey. (2008). The combination of granulocyte colony-stimulating factor and stem cell factor signif cantly increases the number of bone marrow-derived endothelial cells in brains of mice following cerebral ischemia. Blood 111:5544-5552.
55. Le Belle JE, MA Caldwell and CN Svendsen. (2004). Improving the survival of human CNS precursor-derived neruons after transplantation. J Neurosci Res 76:174-183.
56. Yin L, SL Fu, GY Shi, Y Li, JQ Jin, ZW Ma and PH Lu. (2008). Expression and regulation of major histocompatibility complex on neural stem cells and their lineages. Stem Cells Dev 17:53-65.
57. Barzilay R, I Kan, T Ben-Zur, S Bulvik, E Melamed and D Offen. (2008). Induction of human mesenchymal stem cells into dop-amine-producing cells with different differentiation protocols. Stem Cells Dev 17:547-554.
58. Greco SJ, C Zhou, JH Ye and P Rameshwar. (2007). An interdisciplinary approach and characterization of neuronal cells transdifferentiated from human mesenchymal stem cells. Stem Cells Dev 16:811-826.
59. Greschat S, J Schira, P Kury, C Rosenbaum, MA de Souza Silva, G Kogler, P Wernet and HW Muller. (2008). Unrestricted somatic stem cells from human umbilical cord blood can be differentiated into neurons with a dopaminergic phenotype. Stem Cells Dev 17:221-232.
60. Song S, S Song, H Zhang, J Cuevas and J Sanchez-Ramos. (2007). Comparison of neuron-like cells derived from bone marrow stem cells to those differentiated from adult brain neural stem cells. Stem Cells Dev 16:747-756.
61. Borta A and GU Hoglinger. (2007). Dopamine and adult neuro-genesis. J Neurochem 100:587-595.
62. Freundlieb N, C Francois, D Tande, WH Oertel, EC Hirsch and GU Hoglinger. (2006). Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 26:2321-2325.
63. Hoglinger GU, P Rizk, MP Muriel, C Duyckaerts, WH Oertel, I Caille and EC Hirsch. (2004). Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726 -735.
64. Yoshimi K, YR Ren, T Seki, M Yamada, H Ooizumi, M Onodera, Y Saito, S Murayama, H Okano, Y Mizuno and H Mochizuki. (2005). Possibility for neurogenesis in substantia nigra of par-kinsonian brain. Ann Neurol 58:31-40.
65. Kullberg S, H Aldskogius and B Ulfhake. (2001). Microglial activation, emergence of ED1-expressing cells and clusterin upregulation in the aging rat CNS, with special reference to the spinal cord. Brain Res 899:169-186.
66. Kyrkanides S, MK O'Banion, PE Whiteley, JC Daeschner and JA Olschowka. (2001). Enhanced glial activation and expression of specif c CNS inf ammation-related molecules in aged versus young rats following cortical stab injury. J Neuroimmunol 119:269 -277.
67. Tha KK, Y Okuma, H Miyazaki, T Murayama, T Uehara, R Hatakeyama, Y Hayashi and Y Nomura. (2000). Changes in expressions of proinflammatory cytokines IL-1beta, TNF-alpha and IL-6 in the brain of senescence accelerated mouse (SAM) P8. Brain Res 885:25-31.
68. Perry VH, C Cunningham and C Holmes. (2007). Systemic infections and inf ammation affect chronic neurodegeneration. Nat Rev Immunol 7:161-167.
69. Emerich DF, P Schneider, B Bintz, J Hudak and CG Thanos. (2007). Aging reduces the neuroprotective capacity, VEGF secretion, and metabolic activity of rat choroid plexus epithelial cells. Cell Transplant 16:697-705.
70. Kelly CM, SV Precious, R Penketh, N Amso, SB Dunnett and AE Rosser. (2007). Striatal graft projections are inf uenced by donor cell type and not the immunogenic background. Brain 130:1317-1329.
71. Sarnowska A, M Jurga, L Buzanska, RK Filipkowski, K Duniec and K Domanska-Janik. (2008). Bilateral interaction between cord blood-derived human neural stem cells and organotypic rat hippocampal culture. Stem Cells Dev. [Epub ahead of print]
72. McKenzie JL, OI Gan, M Doedens and JE Dick. (2005). Human short-term repopulating stem cells are efficiently detected following intrafemoral transplantation into NOD/SCID recipients depleted of CD122+ cells. Blood 106:1259-1261.
73. Kozlowska H, J Jablonka, M Janowski, M Jurga, M Kossut and K Domanska-Janik. (2007). Transplantation of a novel human cord blood-derived neural-like stem cell line in a rat model of cortical infarct. Stem Cells Dev 16:481-488.
74. Gao JP, S Sun, WW Li, YP Chen and DF Cai. (2008). Triptolide protects against 1-methyl-4-phenyl pyridinium-induced dopaminergic neurotoxicity in rats: Implication for immuno-suppressive therapy in Parkinson's disease. Neurosci Bull 24:133-142.
75. Morgan D, MN Gordon, J Tan, D Wilcock and AM Rojiani. (2005). Dynamic complexity of the microglial activation response in transgenic models of amyloid deposition: implications for Alzheimer therapeutics. J Neuropathol Exp Neurol 64:743-753.
76. Stromberg I, C Gemma, J Vila and PC Bickford. (2005). Blueberry- and spirulina-enriched diets enhance striatal dopamine recovery and induce a rapid, transient microglia activation after injury of the rat nigrostriatal dopamine system. Exp Neurol 196:298-307.
77. Emerich DF, RL Dean, III and RT Bartus. (2002). The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct? Exp Neurol 173:168-181.
78. Feuerstein G. (2006). Inf ammation and stroke: therapeutic effects of adenoviral expression of secretory Leukocyte Protease Inhibitor. Front Biosci 11:1750-1757.
79. Morganti-Kossmann MC, M Rancan, PF Stahel and T Kossmann. (2002). Inf ammatory response in acute traumatic brain injury: a double-edged sword. Curr Opin Crit Care 8:101-105.
80. Newcomb JD, CT Ajmo, Jr, CD Sanberg, PR Sanberg, KR Pennypacker and AE Willing. (2006). Timing of cord blood treatment after experimental stroke determines therapeutic eff cacy. Cell Transplant 15:213-223.
81. Scherbel U, R Raghupathi, M Nakamura, KE Saatman, JQ Trojanowski, E Neugebauer, MW Marino and TK McIntosh. (1999). Differential acute and chronic responses of tumor necrosis factor-def cient mice to experimental brain injury. Proc Natl Acad Sci USA 96:8721-8726.
82. Carvey PM, A Punati and MB Newman. (2006). Progressive dopamine neuron loss in Parkinson's disease: the multiple hit hypothesis. Cell Transplant 15:239-250.
83. Ling Z, DA Gayle, SY Ma, JW Lipton, CW Tong, JS Hong and PM Carvey. (2002). In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Mov Disord 17:116-124.
84. Ling Z, Y Zhu, C Tong, JA Snyder, JW Lipton and PM Carvey. (2006). Progressive dopamine neuron loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally. Exp Neurol 199:499-512.
85. Koprich JB, C Reske-Nielsen, P Mithal and O Isacson. (2008). Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J Neuroinflammation 5:8.
86. Ohtani Y, M Minami, N Kawaguchi, A Nishiyori, J Yamamoto, S Takami and M Satoh. (1998). Expression of stromal cell-derived factor-1 and CXCR4 chemokine receptor mRNAs in cultured rat glial and neuronal cells. Neurosci Lett 249:163-166.
87. Qin L, X Wu, ML Block, Y Liu, GR Breese, JS Hong, DJ Knapp and FT Crews. (2007). Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453-462.
88. Rankine EL, PM Hughes, MS Botham, VH Perry and LM Felton. (2006). Brain cytokine synthesis induced by an intraparenchymal injection of LPS is reduced in MCP-1-def cient mice prior to leucocyte recruitment. Eur J Neurosci 24:77-86.
89. Bjugstad KB, DE Redmond, Jr, YD Teng, JD Elsworth, RH Roth, BC Blanchard, EY Snyder and JR Sladek, Jr. (2005). Neural stem cells implanted into MPTP-treated monkeys increase the size of endogenous tyrosine hydroxylase-positive cells found in the striatum: a return to control measures. Cell Transplant 14 :18 3 -192 .
90. Emborg ME, AD Ebert, J Moirano, S Peng, M Suzuki, E Capowski, V Joers, BZ Roitberg, P Aebischer and CN Svendsen. (2008). GDNF-secreting human neural progenitor cells increase tyrosine hydroxylase and VMAT2 expression in MPTP-treated cynomolgus monkeys. Cell Transplant 17:383-395.
91. Redmond DE, Jr, KB Bjugstad, YD Teng, V Ourednik, J Ourednik, DR Wakeman, XH Parsons, R Gonzalez, BC Blanchard, SU Kim, Z Gu, SA Lipton, EA Markakis, RH Roth, JD Elsworth, JR Sladek, Jr, RL Sidman and EY Snyder. (2007). Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc Natl Acad Sci USA 104:12175-12180.
92. Sanberg PR. (2007). Neural stem cells for Parkinson's disease: to protect and repair. Proc Natl Acad Sci USA 104:11869-11870.
93. Crigler L, RC Robey, A Asawachaicharn, D Gaupp and DG Phinney. (2006). Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp Neurol 198:54- 64.
94. Einstein O, O Ben-Menachem-Tzidon, R Mizrachi-Kol, E Reinhartz, N Grigoriadis and T Ben-Hur. (2006). Survival of neural precursor cells in growth factor-poor environment: implications for transplantation in chronic disease. Glia 53:449-455.
95. Lee JP, M Jeyakumar, R Gonzalez, H Takahashi, PJ Lee, RC Baek, D Clark, H Rose, G Fu, J Clarke, S McKercher, J Meerloo, FJ Muller, KI Park, TD Butters, RA Dwek, P Schwartz, G Tong, D Wenger, SA Lipton, TN Seyfried, FM Platt and EY Snyder. (2007). Stem cells act through multiple mechanisms to benefit mice with neurodegenerative metabolic disease. Nat Med 13:439-447.
96. Newcomb JD, PR Sanberg, SK Klasko and AE Willing. (2007). Umbilical cord blood research: current and future perspectives. Cell Transplant 16:151-158.
97. Yasuhara T, N Matsukawa, K Hara, G Yu, L Xu, M Maki, SU Kim and CV Borlongan. (2006). Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J Neurosci 26:12497-12511.
98. Hoogduijn MJ, MJ Crop, AM Peeters, GJ Van Osch, AH Balk, JN Ijzermans, W Weimar and CC Baan. (2007). Human heart, spleen, and perirenal fat-derived mesenchymal stem cells have immunomodulatory capacities. Stem Cells Dev 16:597-604.
99. Capone C, S Frigerio, S Fumagalli, M Gelati, MC Principato, C Storini, M Montinaro, R Kraftsik, M De Curtis, E Parati and MG De Simoni. (2007). Neurosphere-derived cells exert a neu-roprotective action by changing the ischemic microenvironment. PLoS ONE 2:e373.
100. Dass B, CW Olanow and JH Kordower. (2006). Gene transfer of trophic factors and stem cell grafting as treatments for Parkinson's disease. Neurology 66:S89-S103.
101. Taylor RM, JP Lee, JJ Palacino, KA Bower, J Li, MT Vanier, DA Wenger, RL Sidman and EY Snyder. (2006). Intrinsic resistance of neural stem cells to toxic metabolites may make them well suited for cell non-autonomous disorders: evidence from a mouse model of Krabbe leukodystrophy. J Neurochem 97:1585-1599.
102. Husseini L, T Schmandt, B Scheffler, W Schroder, G Seifert, O Brustle and C Steinhauser. (2008). Functional analysis of embryonic stem cell-derived glial cells after integration into hippocampal slice cultures. Stem Cells Dev 17:1141-1152.
103. Feigin A, MG Kaplitt, C Tang, T Lin, P Mattis, V Dhawan, MJ During and D Eidelberg. (2007). Modulation of metabolic brain networks after subthalamic gene therapy for Parkinson's disease. Proc Natl Acad Sci USA 104:19559-19564.
104. Kaplitt MG, A Feigin, C Tang, HL Fitzsimons, P Mattis, PA Lawlor, RJ Bland, D Young, K Strybing, D Eidelberg and MJ During. (2007). Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369:2097-2105.
105. McRae C, E Cherin, TG Yamazaki, G Diem, AH Vo, D Russell, JH Ellgring, S Fahn, P Greene, S Dillon, H Winf eld, KB Bjugstad and CR Freed. (2004). Effects of perceived treatment on quality of life and medical outcomes in a double-blind placebo surgery trial. Arch Gen Psychiatry 61:412-420.