Therapeutic effect of BDNF-overexpressing human neural stem cells (HB1.F3.BDNF) in a rodent model of middle cerebral artery occlusion

Cell Transplantation

Volumn 22, Issue 8, 2013, Pages 1441-1452

  Chang, Da Jeong ^a   Lee, Nayeon ^a   Choi, Chunggab ^a   Jeon, Iksoo ^a   Oh, Seung Hun ^a   Shin, Dong Ah ^b   Hwang, Tae Sun ^a   Lee, Hong J ^c   Kim, Seung U ^c   Moon, Hyeyoung ^d   Hong, Kwan Soo ^d   Kang, Kyung Sun ^e   Song, Jihwan ^a  

^a CHA University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Chung Ang University College of Medicine   (South Korea)

^d Korea Basic Science Institute (KBSI)   (South Korea)

^e Seoul National University   (South Korea)

Author keywords

Animal MRI; Behavioral recovery; Brain derived neurotrophic factor (BDNF); Neural stem cells (NSCs); Stroke

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; PHOSPHOPROTEIN DARPP 32;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CELL MIGRATION; CLINICAL ASSESSMENT TOOL; CONTROLLED STUDY; CONVALESCENCE; CORPUS STRIATUM; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MIDDLE CEREBRAL ARTERY OCCLUSION; MODIFIED NEUROLOGICAL SEVERITY SCORE; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THERAPY EFFECT; WESTERN BLOTTING;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL LINE; CELL MOVEMENT; CELL TRACKING; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; MAGNETIC RESONANCE IMAGING; MALE; MODELS, BIOLOGICAL; NEURAL STEM CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84881004658     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X657323     Document Type: Article

References (39)

1. Aboody, K.; Capela, A.; Niazi, N.; Stern, J. H.; Temple, S. Translating stem cell studies to the clinic for CNS repair: Current state of the art and the need for a rosetta stone. Neuron 70:597-613; 2011.
2. Andsberg, G.; Kokaia, Z.; Klein, R. L.; Muzyczka, N.; Lindvall, O.; Mandel, R. J. Neuropathological and behavioral consequences of adeno-associated viral vector-mediated continuous intrastriatal neurotrophin delivery in a focal ischemia model in rats. Neurobiol. Dis. 9:187-204; 2002.
3. Arvidsson, A.; Collin, T.; Kirik, D.; Kokaia, Z.; Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8:963-970; 2002.
4. Bang, O. Y.; Lee, J. S.; Lee, P. H.; Lee, G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann. Neurol. 57:874-882; 2005.
5. Bederson, J. B.; Pitts, L. H.; Tsuji, M.; Nishimura, M. C.; Davis, R. L.; Bartkowski, H. Rat middle cerebral artery occlusion: Evaluation of the model and development of a neurologic examination. Stroke 17:472-476; 1986.
6. Chang, D. J.; Moon, H.; Lee, Y. H.; Lee, N.; Lee, H. J.; Jeon, I.; Lee, H.; Hwang, T. S.; Oh, S. H.; Shin, D. A.; Kim, S. U.; Hong, K. S.; Song, J. In vivo tracking of human neural stem cells following transplantation into a rodent model of ischemic stroke. Int. J. Stem Cells 5:81-85; 2012.
7. Cho, T.; Bae, J. H.; Choi, H. B.; Kim, S. S.; McLarnon, J. G.; Kim, S. U. Human neural stem cells: Electrophysiological properties of voltage gated ion channels. Neuroreport 13:1447-1452; 2002.
8. Chu, K.; Kim, M.; Jeong, S. W.; Kim, S. U.; Yoon, B. W., Human neural stem cells can migrate, differentiate, and integrate after intravenous transplantation in adult rats with transient forebrain ischemia. Neurosci. Lett. 343:129-133; 2003.
9. Chu, K.; Kim, M.; Park, K. I.; Jeong, S. W.; Park, H. K.; Jun, K. H.; Lee, S. T.; Kang, L.; Lee, K.; Park, D. K.; Kim, S. U.; Roh, J. K. Human neural stem cells improve sensorimotor deficits in the rat brain with experimental focal ischemia. Brain Res. 1016:145-153; 2004.
10. De Ryck, M.; Van Reempts, J.; Borgers, M.; Wauquier, A.; Janssen, P. A. Photochemical stroke model: Flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 20:1383-1390; 1989.
11. Honmou, O.; Houkin, K.; Matsunaga, T.; Niitsu, Y.; Ishiai, S.; Onodera, R.; Waxman, S. G.; Kocsis, J. D. Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain 134:1790-1807; 2011.
12. Huang, E. J.; Reichardt, L. F. Neurotrophins: Roles in neuronal development and function. Annu. Rev. Neurosci. 24: 677-736; 2001.
13. Imitola, J.; Raddassi, K.; Park, K. I.; Mueller, F. J.; Nieto, M.; Teng, Y. D.; Frenkel, D.; Li, J.; Sidman, R. L.; Walsh, C. A.; Snyder, E. Y.; Khoury, S. J. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1 a/CXC chemokine receptor 4 pathway. Proc. Natl. Acad. Sci. USA 101:18117-122; 2004.
14. Jeong, S. W.; Chu, K.; Jung, K. H., Kim, S. U.; Kim, M.; Roh, J. K. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 34: 2258-2263; 2003.
15. Kelly, S.; Bliss, T. M.; Shah, A. K.; Sun, G. H.; Ma, M.; Foo, W. C.; Masel, J.; Yenari, M. A.; Weissman, I. L.; Uchida, N., Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc. Natl. Acad. Sci. USA 101:11839-11844; 2004.
16. Kim, D.; Chun, B. G.; Kim, Y. G.; Lee, Y. H.; Park, C. S.; Jeon, I.; Cheong, C.; Hwang, T. S.; Chung, H.; Gwag, B. J.; Hong, K. S.; Song, J. In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant. 16:1007-1012; 2007.
17. Kim, S. U.; deVellis, J. Stem cell-based cell therapy in neurological diseases: A review. J. Neurosci. Res. 88: 2183-2200; 2009.
18. Kim, S. U.; Nagai, A.; Nakagawa, E.; Choi, H. B.; Bang, J. H.; Lee, H. J.; Lee, M. A.; Lee, Y. B.; Park, I. H. Production and characterization of immortal human neural stem cell line with multipotent differentiation property. Methods Mol. Biol. 438:103-121; 2008.
19. Kondziolka, D.; Steinberg, G. K.; Wechsler, L.; Meltzer, C. C.; Elder, E.; Gebel, J.; Decesare, S.; Jovin, T.; Zafonte, R.; Lebowitz, J.; Flickinger, J. C.; Tong, D.; Marks, M. P.; Jamieson, C.; Luu, D.; Bell-Stephens, T.; Teraoka, J. Neurotransplantation for patients with subcortical motor stroke: A phase 2 randomized trial. J. Neurosurg. 103: 38-45; 2005.
20. Kondziolka, D.; Wechsler, L.; Goldstein, S.; Meltzer, C.; Thulborn, K. R.; Gebel, J.; Jannetta, P.; DeCesare, S.; Elder, E. M.; McGrogan, M.; Reitman, M. A.; Bynum, L. Transplantation of cultured human neuronal cells for patients with stroke. Neurology 55:565-569; 2000.
21. Kurozumi, K.; Nakamura, K.; Tamiya, T.; Kawano, Y.; Kobune, M.; Hirai, S.; Uchida, H.; Sasaki, K.; Ito, Y.; Kato, K.; Honmou, K.; Date, I.; Hamada, H. BDNF gene-modified mesenchymal stem cells promote functional recovery and reduce infarct size in the rat middle cerebral artery occlusion model. Mol. Ther. 9:189-197; 2004.
22. Lee, H. J.; Kim, K. S.; Kim, E. J.; Lee, K. H.; Choi, H. B.; Ko, Y.; Jeong, S. W.; Kim, S. U. Brain transplantation of human neural stem cells promotes functional recovery in mouse intracerebral hemorrhage stroke model. Stem Cells 25:211-224; 2007.
23. Lee, H. J.; Lim, I. J.; Lee, M. C.; Kim, S. U. Human neural stem cells genetically modified to overexpress brain-derived neurotrophic factor promote functional recovery and neuroprotection in a mouse stroke model. J. Neurosci. Res. 88:3282-3294; 2010.
24. Lindvall, O.; Ernfors, P.; Bengzon, J.; Kokaia, Z.; Smith, M. L.; Siesjö, B. K.; Persson, H. S. Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. Natl. Acad. Sci. USA 89:648-652; 1992.
25. Lindvall, O.; Kokaia, Z. Stem cell research in stroke: How far from the clinic? Stroke 42(8):2369-2375; 2011.
26. Lindvall, O.; Kokaia, Z. Stem cells for the treatment of neurological disorders. Nature 441:1094-1096; 2006.
27. Lindvall, O.; Kokaia, Z. Stem cells in human neurodegenerative disorders-time for clinical translation? J. Clin. Invest. 120:29-40; 2010.
28. Longa, E. Z.; Weinstein, P. R.; Carlson, S.; Cummins, R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91; 1989.
29. Miller, R. J.; Banisadr, G.; Bhattacharyya, B. J. CXCR4 signaling in the regulation of stem cell migration and development. J. Neuroimmunol. 198:31-38; 2008.
30. Nelson, P. T.; Kondziolka, D.; Wechsler, L.; Goldstein, S.; Gebel, J.; DeCesare, S.; Elder, E. M.; Zhang, P. J.; Jacobs, A.; McGrogan, M.; Lee, V. M.; Trojanowski, J. Q. Clonal human (hNT) neuron grafts for stroke therapy: Neuropathology in a patient 27 months after implantation. Am. J. Pathol. 160:1201-1206; 2002.
31. Nomura, T.; Honmou, O.; Harada, K.; Houkin, K.; Hamada, H.; Kocsis, J. D. IV infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience 136:161-169; 2005.
32. Olsson, M.; Nikkhah, G.; Bentlage, C.; Björklund, A. Forelimb akinesia in the rat Parkinson model: Differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15:3863-3875; 1995.
33. Pollock, K.; Stremer, P.; Patel, S.; Stevanato, L.; Hope, A.; Miljan, E.; Dong, Z.; Hodges, H.; Price, J.; Sinden, J. D. A conditionally immortal clonal stem cell line from human cortical neuroepithelium for the treatment of ischemic stroke. Exp. Neurol. 199:143-155; 2006.
34. Reglodi, D.; Tamás, A.; Lengvári, I. Examination of sensorimotor performance following middle cerebral artery occlusion in rats Brain. Res. Bull. 59:459-466; 2003.
35. Sanberg, P. R.; Eve, D. J.; Cruz, L. E.; Borlongan, C. V. Neurological disorders and the potential role for stem cells as a therapy. Br. Med. Bull. 101:163-181; 2012.
36. Schabitz, W. R.; Steigleder, T.; Cooper-Kuhn, C. M.; Schwab, S.; Sommer, C.; Schnider, A.; Kuhn, H. G. Intravenous BDNF enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke 38:2165-2172; 2007.
37. Ungerstedt, U.; Arbuthnott, G. W. Quantitative recording of rotational behavior in rats after 6-hydroxydopamine lesions of the nigrostriatal dopamine system. Brain Res. 24:485-493; 1970.
38. Yamashita, K.; Wiessner, C.; Lindholm, D.; Thoenen, H.; Hossmann, K. A. Post-occulusion treatment with BDNF reduces infarct size in a model of permanent occulusion of the middle artery in rat. Metab. Brain Dis. 12:271-280; 1997.
39. Zhang, Z. G.; Chopp, M. Neurorestorative therapies for stroke: Underlying mechanisms and translation to the clinic. Lancet Neurol. 8:491-500; 2009.