Neural stem cells improve memory in an inducible mouse model of neuronal loss

Journal of Neuroscience

Volumn 27, Issue 44, 2007, Pages 11925-11933

  Yamasaki, Tritia R ^a   Blurton Jones, Mathew ^a   Morrissette, Debbi A ^a   Kitazawa, Masashi ^a   Oddo, Salvatore ^a   LaFerla, Frank M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ablation; Functional recovery; Memory; Neuronal death; Stem cells; Transgenic

Indexed keywords

DIPHTHERIA TOXIN; TETRACYCLINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL LOSS; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE MODEL; HIPPOCAMPUS; MEMORY DISORDER; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; THERAPY EFFECT; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN DISEASES; BROMODEOXYURIDINE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; DIPHTHERIA TOXIN; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; IN SITU NICK-END LABELING; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; NEURONS; PEPTIDE FRAGMENTS; PHOSPHOPYRUVATE HYDRATASE; STEM CELL TRANSPLANTATION; TETRACYCLINE;

EID: 35948979698     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1627-07.2007     Document Type: Article

References (48)

1. Auerbach JM, Eiden MV, McKay RD (2000) Transplanted CNS stem cells form functional synapses in vivo. Eur J Neurosci 12:1696-1704.
2. Bernreuther C, Dihne M, Johann V, Schiefer J, Cui Y, Hargus G, Schmid JS, Xu J, Kosinski CM, Schachner M (2006) Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J Neurosci 26:11532-11539.
3. Bramlett HM, Dietrich WD (2004) Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J Cereb Blood Flow Metab 24:133-150.
4. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2:51-61.
5. Buffalo EA, Reber PJ, Squire LR (1998) The human perirhinal cortex and recognition memory. Hippocampus 8:330-339.
6. Cao Q, Benton RL, Whittemore SR (2002) Stem cell repair of central nervous system injury. J Neurosci Res 68:501-510.
7. Carmichael ST (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2:396-409.
8. Causing CG, Gloster A, Aloyz R, Bamji SX, Chang E, Fawcett J, Kuchel G, Miller FD (1997) Synaptic innervation density is regulated by neuron-derived BDNF. Neuron 18:257-267.
9. Cummings BJ, Uchida N, Tamaki SJ, Salazar DL, Hooshmand M, Summers R, Gage FH, Anderson AJ (2005) Human neural stem cells differentiate and promote locomotor recovery in spinal cord-injured mice. Proc Natl Acad Sci USA 102:14069-14074.
10. Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41-50.
11. Englund U, Bjorklund A, Wictorin K, Lindvall O, Kokaia M (2002) Grafted neural stem cells develop into functional pyramidal neurons and integrate into host cortical circuitry. Proc Natl Acad Sci USA 99:17089-17094.
12. Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31:47-59.
13. Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. San Diego: Academic.
14. Gao J, Prough DS, McAdoo DJ, Grady JJ, Parsley MO, Ma L, Tarensenko YI, Wu P (2006) Transplantation of primed human fetal neural stem cells improves cognitive function in rats after traumatic brain injury. Exp Neurol 201:281-292.
15. Gould E, Tanapat P (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80:427-436.
16. Hoane MR, Becerra GD, Shank JE, Tatko L, Pak ES, Smith M, Murashov AK (2004) Transplantation of neuronal and glial precursors dramatically improves sensorimotor function but not cognitive function in the traumatically injured brain. J Neurotrauma 21:163-174.
17. Hoehn M, Kustermann E, Blunk J, Wiedermann D, Trapp T, Wecker S, Focking M, Arnold H, Hescheler J, Fleischmann BK, Schwindt W, Buhrle C (2002) Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci USA 99:16267-16272.
18. Jarrard LE (2002) Use of excitotoxins to lesion the hippocampus: update. Hippocampus 12:405-414.
19. Jeltsch H, Yee J, Aloy E, Marques Pereira P, Schimchowitsch S, Grandbarbe L, Caillard S, Mohier E, Cassel JC (2003) Transplantation of neurospheres after granule cell lesions in rats: cognitive improvements despite no long-term immunodetection of grafted cells. Behav Brain Res 143:177-191.
20. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 98:4710-4715.
21. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, Bredesen DE, Greenberg DA (2004) Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc Natl Acad Sci USA 101:13363-13367.
22. Kelly S, Bliss TM, Shah AK, Sun GH, Ma M, Foo WC, Masel J, Yenari MA, Weissman IL, Uchida N, Palmer T, Steinberg GK (2004) Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex. Proc Natl Acad Sci USA 101:11839-11844.
23. Kochi SK, Collier RJ (1993) DNA fragmentation and cytolysis in U937 cells treated with diphtheria toxin or other inhibitors of protein synthesis. Exp Cell Res 208:296-302.
24. Kokaia Z, Andsberg G, Yan Q, Lindvall O (1998) Rapid alterations of BDNF protein levels in the rat brain after focal ischemia: evidence for increased synthesis and anterograde axonal transport. Exp Neurol 154:289-301.
25. Lee P, Morley G, Huang Q, Fischer A, Seiler S, Horner JW, Factor S, Vaidya D, Jalife J, Fishman GI (1998) Conditional lineage ablation to model human diseases. Proc Natl Acad Sci USA 95:11371-11376.
26. Lindvall O, Kokaia Z (2006) Stem cells for the treatment of neurological disorders. Nature 441:1094-1096.
27. Lindvall O, Kokaia Z, Martinez-Serrano A (2004) Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med [Suppl] 10:S42-S50.
28. Llado J, Haenggeli C, Maragakis NJ, Snyder EY, Rothstein JD (2004) Neural stem cells protect against glutamate-induced excitotoxicity and promote survival of injured motor neurons through the secretion of neurotrophic factors. Mol Cell Neurosci 27:322-331.
29. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
30. Mizumoto H, Mizumoto K, Shatos MA, Klassen H, Young MJ (2003) Retinal transplantation of neural progenitor cells derived from the brain of GFP transgenic mice. Vision Res 43:1699-1708.
31. Morrison JH, Hof PR (1997) Life and death of neurons in the aging brain. Science 278:412-419.
32. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H (2002) Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9:49-57.
33. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y (1997) "Green mice" as a source of ubiquitous green cells. FEBS Lett 407:313-319.
34. Oliveira Jr AA, Hodges HM (2005) Alzheimer's disease and neural transplantation as prospective cell therapy. Curr Alzheimer Res 2:79-95.
35. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
36. Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159-4167.
37. Polito A, Reynolds R (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707-716.
38. Shear DA, Tate MC, Archer DR, Hoffman SW, Hulce VD, Laplaca MC, Stein DG (2004) Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res 1026:11-22.
39. Toda H, Takahashi J, Iwakami N, Kimura T, Hoki S, Mozumi-Kitamura K, Ono S, Hashimoto N (2001) Grafting neural stem cells improved the impaired spatial recognition in ischemic rats. Neurosci Lett 316:9-12.
40. Tuszynski MH, Gage FH (1995) Maintaining the neuronal phenotype after injury in the adult CNS. Neurotrophic factors, axonal growth substrates, and gene therapy. Mol Neurobiol 10:151-167.
41. Veizovic T, Beech JS, Stroemer RP, Watson WP, Hodges H (2001) Resolution of stroke deficits following contralateral grafts of conditionally immortal neuroepithelial stem cells. Stroke 32:1012-1019.
42. Vora N, Jovin T, Kondziolka D (2006) Cell transplantation for ischemic stroke. Neurodegener Dis 3:101-105.
43. Vroemen M, Weidner N, Blesch A (2005) Loss of gene expression in lentivirus- and retrovirus-transduced neural progenitor cells is correlated to migration and differentiation in the adult spinal cord. Exp Neurol 195:127-139.
44. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24:5901-5908.
45. Yasuhara T, Matsukawa N, Hara K, Yu G, Xu L, Maki M, Kim SU, Borlongan CV (2006) Transplantation of human neural stem cells exerts neuroprotection in a rat model of Parkinson's disease. J Neurosci 26:12497-12511.
46. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98:5874-5879.
47. Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11:234-245.
48. Ziv Y, Avidan H, Pluchino S, Martino G, Schwartz M (2006) Synergy between immune cells and adult neural stem/progenitor cells promotes functional recovery from spinal cord injury. Proc Natl Acad Sci USA 103:13174-13179.