Sustained mobilization of endogenous neural progenitors delays disease progression in a transgenic model of huntington's disease

Cell Stem Cell

Volumn 12, Issue 6, 2013, Pages 787-799

  Benraiss, Abdellatif ^a   Toner, Michael J ^a   Xu, Qiwu ^a   Bruel Jungerman, Elodie ^a   Rogers, Eloise H ^a   Wang, Fushun ^a   Economides, Aris N ^b   Davidson, Beverly L ^c   Kageyama, Ryoichiro ^d   Nedergaard, Maiken ^a   Goldman, Steven A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BROXURIDINE; DOUBLECORTIN; ENKEPHALIN; NOGGIN; PHOSPHOPROTEIN DARPP 32; SUBSTANCE P; TAMOXIFEN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL NUCLEUS INCLUSION BODY; COMPARATIVE STUDY; CONTROLLED STUDY; DETERIORATION; DISEASE COURSE; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; EPENDYMA CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; FOREBRAIN; GENE EXPRESSION; GLOBUS PALLIDUS; HEART VENTRICLE WALL; HUNTINGTON CHOREA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; LIFESPAN; MEMBRANE STEADY POTENTIAL; MOTOR PERFORMANCE; MOUSE; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; SQUIRREL MONKEY; STEM CELL; STEM CELL MOBILIZATION; STEREOMETRY; SUBVENTRICULAR ZONE; SURVIVAL; TRANSGENE; VIRUS GENOME; WEIGHT REDUCTION; WILD TYPE; ANIMAL; CYTOLOGY; DISEASE MODEL; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ADENO-ASSOCIATED VIRUS; MUS; SAIMIRI;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS;

EID: 84878847875     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.04.014     Document Type: Article

References (44)

1. V.M. André, C. Cepeda, Y.E. Fisher, M. Huynh, N. Bardakjian, S. Singh, X.W. Yang, and M.S. Levine Differential electrophysiological changes in striatal output neurons in Huntington's disease J. Neurosci. 31 2011 1170 1182
2. G. Bates Huntingtin aggregation and toxicity in Huntington's disease Lancet 361 2003 1642 1644
3. M.W. Becher, J.A. Kotzuk, A.H. Sharp, S.W. Davies, G.P. Bates, D.L. Price, and C.A. Ross Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length Neurobiol. Dis. 4 1998 387 397
4. A. Bedard, C. Gravel, and A. Parent Chemical characterization of newly generated neurons in the striatum of adult primates Exp. Brain Res. 170 2005 501 512
5. L. Bekar, W. Libionka, G.F. Tian, Q. Xu, A. Torres, X. Wang, D. Lovatt, E. Williams, T. Takano, and J. Schnermann Adenosine is crucial for deep brain stimulation-mediated attenuation of tremor Nat. Med. 14 2008 75 80
6. A. Benraiss, and S.A. Goldman Cellular therapy and induced neuronal replacement for Huntington's disease Neurotherapeutics 8 2011 577 590
7. A. Benraiss, E. Chmielnicki, K. Lerner, D. Roh, and S.A. Goldman Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain J. Neurosci. 21 2001 6718 6731
8. A. Benraiss, E. Bruel-Jungerman, G. Lu, A.N. Economides, B. Davidson, and S.A. Goldman Sustained induction of neuronal addition to the adult rat neostriatum by AAV4-delivered noggin and BDNF Gene Ther. 19 2012 483 493
9. E. Chmielnicki, A. Benraiss, A.N. Economides, and S.A. Goldman Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone J. Neurosci. 24 2004 2133 2142
10. S.R. Cho, A. Benraiss, E. Chmielnicki, A. Samdani, A. Economides, and S.A. Goldman Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease J. Clin. Invest. 117 2007 2889 2902
11. C.W. Christine, P.A. Starr, P.S. Larson, J.L. Eberling, W.J. Jagust, R.A. Hawkins, H.F. VanBrocklin, J.F. Wright, K.S. Bankiewicz, and M.J. Aminoff Safety and tolerability of putaminal AADC gene therapy for Parkinson disease Neurology 73 2009 1662 1669
12. M.A. Curtis, E.B. Penney, A.G. Pearson, W.M. van Roon-Mom, N.J. Butterworth, M. Dragunow, B. Connor, and R.L. Faull Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain Proc. Natl. Acad. Sci. USA 100 2003 9023 9027
13. Y. Dai, E.M. Schwarz, D. Gu, W.W. Zhang, N. Sarvetnick, and I.M. Verma Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression Proc. Natl. Acad. Sci. USA 92 1995 1401 1405
14. B.L. Davidson, C.S. Stein, J.A. Heth, I. Martins, R.M. Kotin, T.A. Derksen, J. Zabner, A. Ghodsi, and J.A. Chiorini Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system Proc. Natl. Acad. Sci. USA 97 2000 3428 3432
15. S.W. Davies, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, C.A. Ross, E. Scherzinger, E.E. Wanker, L. Mangiarini, and G.P. Bates Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
16. J.C. Dodge, C.M. Treleaven, J.A. Fidler, M. Hester, A. Haidet, C. Handy, M. Rao, A. Eagle, J.C. Matthews, and T.V. Taksir AAV4-mediated expression of IGF-1 and VEGF within cellular components of the ventricular system improves survival outcome in familial ALS mice Mol. Ther. 18 2010 2075 2084
17. M. Gray, D.I. Shirasaki, C. Cepeda, V.M. André, B. Wilburn, X.H. Lu, J. Tao, I. Yamazaki, S.H. Li, and Y.E. Sun Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice J. Neurosci. 28 2008 6182 6195
18. C.-A. Gutekunst, F. Norflus, and S.M. Hersch The neuropathology of Huntington's Disease G. Bates, P. Harper, L. Jones, Huntington's Disease 2002 Oxford Oxford 251 275
19. R.A. Henry, S.M. Hughes, and B. Connor AAV-mediated delivery of BDNF augments neurogenesis in the normal and quinolinic acid-lesioned adult rat brain Eur. J. Neurosci. 25 2007 3513 3525
20. M.A. Hickey, and M.F. Chesselet Apoptosis in Huntington's disease Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 255 265
21. I. Imayoshi, T. Ohtsuka, D. Metzger, P. Chambon, and R. Kageyama Temporal regulation of Cre recombinase activity in neural stem cells Genesis 44 2006 233 238
22. I. Imayoshi, M. Sakamoto, T. Ohtsuka, K. Takao, T. Miyakawa, M. Yamaguchi, K. Mori, T. Ikeda, S. Itohara, and R. Kageyama Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain Nat. Neurosci. 11 2008 1153 1161
23. J. Kang, L. Jiang, S.A. Goldman, and M. Nedergaard Astrocyte-mediated potentiation of inhibitory synaptic transmission Nat. Neurosci. 1 1998 683 692
24. H.M. Keyoung, N.S. Roy, A. Benraiss, A. Louissaint Jr., A. Suzuki, M. Hashimoto, W.K. Rashbaum, H. Okano, and S.A. Goldman High-yield selection and extraction of two promoter-defined phenotypes of neural stem cells from the fetal human brain Nat. Biotechnol. 19 2001 843 850
25. B. Kirschenbaum, M. Nedergaard, A. Preuss, K. Barami, R.A. Fraser, and S.A. Goldman In vitro neuronal production and differentiation by precursor cells derived from the adult human forebrain Cereb. Cortex 4 1994 576 589
26. G.J. Klapstein, R.S. Fisher, H. Zanjani, C. Cepeda, E.S. Jokel, M.F. Chesselet, and M.S. Levine Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice J. Neurophysiol. 86 2001 2667 2677
27. U. Lendahl, L.B. Zimmerman, and R.D. McKay CNS stem cells express a new class of intermediate filament protein Cell 60 1990 585 595
28. P.A. LeWitt, A.R. Rezai, M.A. Leehey, S.G. Ojemann, A.W. Flaherty, E.N. Eskandar, S.K. Kostyk, K. Thomas, A. Sarkar, and M.S. Siddiqui AAV2-GAD gene therapy for advanced Parkinson's disease: a double-blind, sham-surgery controlled, randomised trial Lancet Neurol. 10 2011 309 319
29. G. Liu, I.H. Martins, J.A. Chiorini, and B.L. Davidson Adeno-associated virus type 4 (AAV4) targets ependyma and astrocytes in the subventricular zone and RMS Gene Ther. 12 2005 1503 1508
30. L. Madisen, T.A. Zwingman, S.M. Sunkin, S.W. Oh, H.A. Zariwala, H. Gu, L.L. Ng, R.D. Palmiter, M.J. Hawrylycz, and A.R. Jones A robust and high-throughput Cre reporting and characterization system for the whole mouse brain Nat. Neurosci. 13 2010 133 140
31. L. Mangiarini, K. Sathasivam, M. Seller, B. Cozens, A. Harper, C. Hetherington, M. Lawton, Y. Trottier, H. Lehrach, S.W. Davies, and G.P. Bates Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice Cell 87 1996 493 506
32. C.A. Meade, Y.P. Deng, F.R. Fusco, N. Del Mar, S. Hersch, D. Goldowitz, and A. Reiner Cellular localization and development of neuronal intranuclear inclusions in striatal and cortical neurons in R6/2 transgenic mice J. Comp. Neurol. 449 2002 241 269
33. J.L. Mignone, V. Kukekov, A.S. Chiang, D. Steindler, and G. Enikolopov Neural stem and progenitor cells in nestin-GFP transgenic mice J. Comp. Neurol. 469 2004 311 324
34. C. Mueller, and T.R. Flotte Clinical gene therapy using recombinant adeno-associated virus vectors Gene Ther. 15 2008 858 863
35. S. Paine-Saunders, B.L. Viviano, A.N. Economides, and S. Saunders Heparan sulfate proteoglycans retain Noggin at the cell surface: a potential mechanism for shaping bone morphogenetic protein gradients J. Biol. Chem. 277 2002 2089 2096
36. D.W. Pincus, H.M. Keyoung, C. Harrison-Restelli, R.R. Goodman, R.A. Fraser, M. Edgar, S. Sakakibara, H. Okano, M. Nedergaard, and S.A. Goldman Fibroblast growth factor-2/brain-derived neurotrophic factor-associated maturation of new neurons generated from adult human subependymal cells Ann. Neurol. 43 1998 576 585
37. V. Reumers, C.M. Deroose, O. Krylyshkina, J. Nuyts, M. Geraerts, L. Mortelmans, R. Gijsbers, C. Van den Haute, Z. Debyser, and V. Baekelandt Noninvasive and quantitative monitoring of adult neuronal stem cell migration in mouse brain using bioluminescence imaging Stem Cells 26 2008 2382 2390
38. N. Sanai, A.D. Tramontin, A. Quiñones-Hinojosa, N.M. Barbaro, N. Gupta, S. Kunwar, M.T. Lawton, M.W. McDermott, A.T. Parsa, and J. Manuel-García Verdugo Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration Nature 427 2004 740 744
39. F.J. Sim, J. Lang, B. Waldau, N.S. Roy, T. Schwartz, K. Chandross, S. Natesan, J. Merrill, and S.A. Goldman Complementary patterns of gene expression by human oligodendrocyte progenitor cells and their environment predict determinants of progenitor maintenance and differentiation Annals Neurol. 59 2006 763 779
40. A.L. Southwell, S.C. Warby, J.B. Carroll, C.N. Doty, N.H. Skotte, W. Zhang, E.B. Villanueva, V. Kovalik, Y. Xie, and M.A. Pouladi A fully humanized transgenic mouse model of Huntington disease Hum. Mol. Genet. 22 2013 18 34
41. Y. Tamura, Y. Kataoka, Y. Cui, Y. Takamori, Y. Watanabe, and H. Yamada Multi-directional differentiation of doublecortin- and NG2-immunopositive progenitor cells in the adult rat neocortex in vivo Eur. J. Neurosci. 25 2007 3489 3498
42. M. Turmaine, A. Raza, A. Mahal, L. Mangiarini, G.P. Bates, and S.W. Davies Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease Proc. Natl. Acad. Sci. USA 97 2000 8093 8097
43. L. Yu-Taeger, E. Petrasch-Parwez, A.P. Osmand, A. Redensek, S. Metzger, L.E. Clemens, L. Park, D. Howland, C. Calaminus, and X. Gu A novel BACHD transgenic rat exhibits characteristic neuropathological features of Huntington disease J. Neurosci. 32 2012 15426 15438
44. L. Zimmerman, B. Parr, U. Lendahl, M. Cunningham, R. McKay, B. Gavin, J. Mann, G. Vassileva, and A. McMahon Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors Neuron 12 1994 11 24