Functional recovery and neuronal regeneration of a rat model of epilepsy by transplantation of Hes1-down regulated bone marrow stromal cells

Neuroscience

Volumn 212, Issue , 2012, Pages 214-224

  Long, Q ^a,b   Qiu, B ^c   Liu, W ^a   Fei, Z ^a   Feng, G ^b   Wang, P ^b   Zhong, J ^a   Yi, X ^a   Liu, Y ^a   Zhang, Y ^a   Han, R ^d  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b Central Hospital of xi'An   (China)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d Armed Police Hospital of Shanxi Province   (China)

Author keywords

Bone marrow stromal cells; Epilepsy; GABAergic cells; Transplantation

Indexed keywords

BROXURIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE 67; NEURON SPECIFIC ENOLASE; PILOCARPINE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CELL DENSITY; CELL DIFFERENTIATION; CELL ISOLATION; CELL TRANSPLANTATION; CONTROLLED STUDY; DOWN REGULATION; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; EPILEPSY; EPILEPTIC DISCHARGE; FUNCTIONAL ASSESSMENT; GABAERGIC SYSTEM; HEMATOPOIETIC STEM CELL; HIPPOCAMPUS; HISTOPATHOLOGY; INCIDENCE; MALE; MORTALITY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECURRENT DISEASE; SEIZURE; STROMA CELL; THERAPY EFFECT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE MARROW TRANSPLANTATION; CELL LINE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPILEPSY; HOMEODOMAIN PROTEINS; MALE; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; STROMAL CELLS;

EID: 84861701524     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.04.002     Document Type: Article

References (57)

1. Abdanipour A., Tiraihi T., Mirnajafi-Zadeh J. Improvement of the pilocarpine epilepsy model in rat using bone marrow stromal cell therapy. Neurol Res 2011, 33:625-632.
2. Alvarez Dolado M., Broccoli V. GABAergic neuronal precursor grafting: implications in brain regeneration and plasticity. Neural Plast 2011, 2011. Article ID 384216. http://dx.doi.org/10.1155/2011/384216.
3. Blumenfeld H., Varghese G.I., Purcaro M.J., Motelow J.E., Enev M., McNally K.A., Levin A.R., Hirsch L.J., Tikofsky R., Zubal I.G., Paige A.L., Spencer S.S. Cortical and subcortical networks in human secondarily generalized tonic-clonic seizures. Brain 2009, 132:999-1012.
4. Calcagnotto M.E., Zipancic I., Piquer-Gil M., Mello L.E., Alvarez-Dolado M. Grafting of GABAergic precursors rescues deficits in hippocampal inhibition. Epilepsia 2010, 51(Suppl. 3):66-70.
5. Chopp M., Li Y. Transplantation of bone marrow stromal cells for treatment of central nervous system diseases. Adv Exp Med Biol 2006, 585:49-64.
6. Costa-Ferro Z.S., Vitola A.S., Pedroso M.F., Cunha F.B., Xavier L.L., Machado D.C., Soares M.B., Ribeiro-dos-Santos R., DaCosta J.C. Prevention of seizures and reorganization of hippocampal functions by transplantation of bone marrow cells in the acute phase of experimental epilepsy. Seizure 2010, 19:84-92.
7. Costa-Ferro Z.S., Vitola A.S., Pedroso M.F., Cunha F.B., Xavier L.L., Machado D.C., Soares M.B., Ribeiro-dos-Santos R., DaCosta J.C. Prevention of seizures and reorganization of hippocampal functions by transplantation of bone marrow cells in the acute phase of experimental epilepsy. Seizure 2011, 19:84-92.
8. Cox C.S., Baumgartner J.E., Harting M.T., Worth L.L., Walker P.A., Shah S.K., Ewing-Cobbs L., Hasan K.M., Day M.C., Lee D., Jimenez F., Gee A. Autologous bone marrow mononuclear cell therapy for severe traumatic brain injury in children. Neurosurgery 2011, 68:588-600.
9. Dedeurwaerdere S., Gilby K., Vonck K., Delbeke J., Boon P., McIntyre D. Vagus nerve stimulation does not affect spatial memory in fast rats, but has both anti-convulsive and pro-convulsive effects on amygdala-kindled seizures. Neuroscience 2006, 140:1443-1451.
10. Deng Y.B., Ye W.B., Hu Z.Z., Yan Y., Wang Y., Takon B.F., Zhou G.Q., Zhou Y.F. Intravenously administered BMSCs reduce neuronal apoptosis and promote neuronal proliferation through the release of VEGF after stroke in rats. Neurol Res 2010, 32:148-156.
11. Ding D.C., Shyu W.C., Lin S.Z. Mesenchymal stem cells. Cell Transplant 2011, 20:5-14.
12. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
13. Duncan J.S., Sander J.W., Sisodiya S.M., Walker M.C. Adult epilepsy. Lancet 2006, 367:1087-1100.
14. Englot D.J., Yang L., Hamid H., Danielson N., Bai X., Marfeo A., Yu L., Gordon A., Purcaro M.J., Motelow J.E., Agarwal R., Ellens D.J., Golomb J.D., Shamy M.C., Zhang H., Carlson C., Doyle W., Devinsky O., Vives K., Spencer D.D., Spencer S.S., Schevon C., Zaveri H.P., Blumenfeld H. Impaired consciousness in temporal lobe seizures: role of cortical slow activity. Brain 2010, 133:3764-3777.
15. Fang M., Lu Y., Chen G.J., Shen L., Pan Y.M., Wang X.F. Increased expression of Sonic hedgehog in temporal lobe epileptic foci in humans and experimental rats. Neuroscience 2011, 182:62-70.
16. Fisher R.S., van Emde Boas W., Blume W., Elger C., Genton P., Lee P., Engel J. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005, 46:470-472.
17. Gharibani P.M., Tiraihi T., Arabkheradmand J. In vitro differentiation of GABAergic cells from bone marrow stromal cells using potassium chloride as inducer. Restor Neurol Neurosci 2010, 28:367-377.
18. Harting M., Jimenez F., Pati S., Baumgartner J., Cox C. Immunophenotype characterization of rat mesenchymal stromal cells. Cytotherapy 2008, 10:243-253.
19. Helms A.W., Gowan K., Abney A., Savage T., Johnson J.E. Overexpression of MATH1 disrupts the coordination of neural differentiation in cerebellum development. Mol Cell Neurosci 2001, 17:671-682.
20. Hesdorffer D.C., Logroscino G., Benn E.K., Katri N., Cascino G., Hauser W.A. Estimating risk for developing epilepsy: a population-based study in Rochester, Minnesota. Neurology 2011, 76:23-27.
21. Hodaie M., Wennberg R.A., Dostrovsky J.O., Lozano A.M. Chronic anterior thalamus stimulation for intractable epilepsy. Epilepsia 2002, 43:603-608.
22. Jacobs M.P., Leblanc G.G., Brooks-Kayal A., Jensen F.E., Lowenstein D.H., Noebels J.L., Spencer D.D., Swann J.W. Curing epilepsy: progress and future directions. Epilepsy Behav 2009, 14:438-445.
23. Kabos P., Kabosova A., Neuman T. Blocking HES1 expression initiates GABAergic differentiation and induces the expression of p21(CIP1/WAF1) in human neural stem cells. J Biol Chem 2002, 277:8763-8766.
24. Kageyama R., Ohtsuka T., Hatakeyama J., Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 2005, 306:343-348.
25. Kang S.K., Lee D.H., Bae Y.C., Kim H.K., Baik S.Y., Jung J.S. Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats. Exp Neurol 2003, 183:355-366.
26. Kriegstein A.R., Pitkanen A. Commentary: the prospect of cell-based therapy for epilepsy. Neurotherapeutics 2009, 6:295-299.
27. Kukko-Lukjanov T.K., Lintunen M., Jalava N., Lauren H.B., Lopez-Picon F.R., Michelsen K.A., Panula P., Holopainen I.E. Involvement of histamine 1 receptor in seizure susceptibility and neuroprotection in immature mice. Epilepsy Res 2010, 90:8-15.
28. Lehmann H., Ebert U., Loscher W. Amygdala-kindling induces a lasting reduction of GABA-immunoreactive neurons in a discrete area of the ipsilateral piriform cortex. Synapse 1998, 29:299-309.
29. Locklin R.M., Riggs B.L., Hicok K.C., Horton H.F., Byrne M.C., Khosla S. Assessment of gene regulation by bone morphogenetic protein 2 in human marrow stromal cells using gene array technology. J Bone Miner Res 2001, 16:2192-2204.
30. Longo B., Romariz S., Blanco M.M., Vasconcelos J.F., Bahia L., Soares M.B., Mello L.E., Ribeiro-dos-Santos R. Distribution and proliferation of bone marrow cells in the brain after pilocarpine-induced status epilepticus in mice. Epilepsia 2010, 51:1628-1632.
31. Loscher W., Schwark W.S. Evidence for impaired GABAergic activity in the substantia nigra of amygdaloid kindled rats. Brain Res 1985, 339:146-150.
32. Madhavan L., Collier T.J. A synergistic approach for neural repair: cell transplantation and induction of endogenous precursor cell activity. Neuropharmacology 2010, 58:835-844.
33. Maisano X., Carpentino J., Becker S., Lanza R., Aaron G., Grabel L., Naegele J.R. Embryonic stem cell-derived neural precursor grafts for treatment of temporal lobe epilepsy. Neurotherapeutics 2009, 6:263-277.
34. Murata K., Hattori M., Hirai N., Shinozuka Y., Hirata H., Kageyama R., Sakai T., Minato N. Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol Cell Biol 2005, 25:4262-4271.
35. Nagai A., Kim W.K., Lee H.J., Jeong H.S., Kim K.S., Hong S.H., Park I.H., Kim S.U. Multilineage potential of stable human mesenchymal stem cell line derived from fetal marrow. PLoS One 2007, 2. e1272-1-18.
36. Naghdi M., Tiraihi T., Mesbah-Namin S.A., Arabkheradmand J. Induction of bone marrow stromal cells into cholinergic-like cells by nerve growth factor. Iran Biomed J 2009, 13:117-123.
37. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Elsevier.
38. Perucca E., Tomson T. The pharmacological treatment of epilepsy in adults. Lancet Neurol 2011, 10:446-456.
39. Polisetti N., Chaitanya V.G., Babu P.P., Vemuganti G.K. Isolation, characterization and differentiation potential of rat bone marrow stromal cells. Neurol India 2010, 58:201-208.
40. Prockop D.J., Phinney D.G., Bunnell B.A. Methods in molecular biology. Mesenchymal Stem Cells: Methods and Protocols 2008, vol. 449. Human Press, New Orleans, LA, p. 171-191.
41. Racine R.J. Modification of seizure activity by electrical stimulation. I: After-discharge threshold. Electroencephalogr Clin Neurophysiol 1972, 32:269-279.
42. Raedt R., Boon P. Cell therapy for neurological disorders: a comprehensive review. Acta Neurol Belg 2005, 105:158-170.
43. Raedt R., Van Dycke A., Vonck K., Boon P. Cell therapy in models for temporal lobe epilepsy. Seizure 2007, 16:565-578.
44. Ren G., Li T., Lan J.Q., Wilz A., Simon R.P., Boison D. Lentiviral RNAi-induced downregulation of adenosine kinase in human mesenchymal stem cell grafts: a novel perspective for seizure control. Exp Neurol 2007, 208:26-37.
45. Ruschenschmidt C., Koch P.G., Brustle O., Beck H. Functional properties of ES cell-derived neurons engrafted into the hippocampus of adult normal and chronically epileptic rats. Epilepsia 2005, 46(Suppl. 5):174-183.
46. Sanabria E.R., D'Andrea Vieira I., da Silveira Pereira M.F., Faria L.C., da Silva A.C., Cavalheiro E.A., da Silva Fernandes M.J. Pro-epileptic effect of alfentanil in rats subjected to pilocarpine-induced chronic epilepsy. Brain Res Bull 2006, 69:535-545.
47. Scardigli R., Schuurmans C., Gradwohl G., Guillemot F. Crossregulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord. Neuron 2001, 31:203-217.
48. Scintu F., Reali C., Pillai R., Badiali M., Sanna M.A., Argiolu F., Ristaldi M.S., Sogos V. Differentiation of human bone marrow stem cells into cells with a neural phenotype: diverse effects of two specific treatments. BMC Neurosci 2006, 7:14. 10.1186/1471-2202-7-14.
49. Shindo A., Nakamura T., Matsumoto Y., Kawai N., Okano H., Nagao S., Itano T., Tamiya T. Seizure suppression in amygdala-kindled mice by transplantation of neural stem/progenitor cells derived from mouse embryonic stem cells. Neurol Med Chir (Tokyo) 2010, 50:98-105. discussion 105-106.
50. Tamminga C., Hashimoto T., Volk D.W., Lewis D.A. GABA neurons in the human prefrontal cortex. Am J Psychiatry 2004, 161:1764.
51. Uccelli A., Prockop D.J. Why should mesenchymal stem cells (MSCs) cure autoimmune diseases?. Curr Opin Immunol 2010, 22:768-774.
52. Vaquero J., Zurita M. Functional recovery after severe CNS trauma: current perspectives for cell therapy with bone marrow stromal cells. Prog Neurobiol 2011, 93:341-349.
53. Vemuri M.C., Chase L.G., Rao M.S. Mesenchymal stem cell assays and applications. Methods Mol Biol 2011, 698:3-8.
54. Venturin G.T., Greggio S., Marinowic D.R., Zanirati G., Cammarota M., Machado D.C., Dacosta J.C. Bone marrow mononuclear cells reduce seizure frequency and improve cognitive outcome in chronic epileptic rats. Life Sci 2011, 89:229-234.
55. Woo N.H., Lu B. Regulation of cortical interneurons by neurotrophins: from development to cognitive disorders. Neuroscientist 2006, 12:43-56.
56. Zipancic I., Calcagnotto M.E., Piquer-Gil M., Mello L.E., Alvarez-Dolado M. Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility. Cell Transplant 2010, 19:549-564.
57. Zurita M., Vaquero J., Bonilla C., Santos M., De Haro J., Oya S., Aguayo C. Functional recovery of chronic paraplegic pigs after autologous transplantation of bone marrow stromal cells. Transplantation 2008, 86:845-853.