[en] Neural and mesenchymal stem cells have been proposed as alternative sources of cells for transplantation into the brain in neurodegenerative disorders. However, the endogenous factors controlling their engraftment within the injured parenchyma remain ill-defined. Here, we demonstrate significant engraftment of undifferentiated exogenous mesenchymal or neural stem cells throughout the lesioned area in a rat model for Huntington's disease, as late as 8 weeks post-transplantation. We show that stem cell factor (SCF), strongly up-regulated within host cells in the damaged striatum, is able to activate the SCF receptor c-kit and its signaling pathway and to promote the migration and proliferation of mesenchymal and neural stem cells in vitro. Furthermore, c-kit receptor blockade alters neural stem cell distribution within the lesioned striatum. Host SCF expression is observed in atypical cells expressing glial fibrillary acidic protein and doublecortin in the lesioned striatum and in migrating doublecortin-positive progenitors. Taken together, these data demonstrate that SCF produced in situ in the lesioned striatum is an important factor in promoting the engraftment of stem cells within the lesioned brain.
Disciplines :
Biochemistry, biophysics & molecular biology Life sciences: Multidisciplinary, general & others
Author, co-author :
Bantubungi, Kadiombo
Blum, David
Cuvelier, Laetitia
Wislet-Gendebien, Sabine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Rogister, Bernard ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman
Brouillet, Emmanuel
Schiffmann, Serge
Language :
English
Title :
Stem cell factor and mesenchymal and neural stem cell transplantation in a rat model of Huntington's disease.
Publication date :
2008
Journal title :
Molecular and Cellular Neuroscience
ISSN :
1044-7431
eISSN :
1095-9327
Publisher :
Academic Press
Volume :
37
Issue :
3
Pages :
454-70
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FNRS (Belgium), FMRE (Belgium), Van Buuren Foundation (Belgium), Action de Recherche Concertée (Communauté Française de Belgique), Hereditary Disease Foundation (USA), the Ligue Belge de la Sclérose en Plaques and the Fonds Charcot.
M. Arango S. Holbert D. Zala E. Brouillet J. Pearson E. Regulier A.K. Thakur P. Aebischer R. Wetzel N. Deglon C. Neri CA150 expression delays striatal cell death in overexpression and knock-in conditions for mutant huntingtin neurotoxicity J. Neurosci. 26 2006 4649 4659
A. Arvidsson T. Collin D. Kirik Z. Kokaia O. Lindvall Neuronal replacement from endogenous precursors in the adult brain after stroke Nat. Med. 8 2002 963 970
DM. Ashley S.J. Bol C. Waugh G. Kannourakis A novel approach to the measurement of different in vitro leukaemic cell growth parameters: the use of PKH GL fluorescent probes Leuk. Res. 17 1993 873 882
A.C. Bachoud-Levi P. Remy J.P. Nguyen P. Brugieres J.P. Lefaucheur C. Bourdet S. Baudic V. Gaura P. Maison B. Haddad M.F. Boisse T. Grandmougin R. Jeny P. Bartolomeo G. Dalla Barba J.D. Degos F. Lisovoski A.M. Ergis E. Pailhous P. Cesaro P. Hantraye M. Peschanski Motor and cognitive improvements in patients with Huntington's disease after neural transplantation Lancet 356 2000 1975 1979
A.C. Bachoud-Levi V. Gaura P. Brugieres M.F. Boisse P. Maison S. Baudic M.J. Ribeiro C. Bourdet P. Remy P. Cesaro P. Hantraye M. Peschanski Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long term follow-up study Lancet Neurol. 5 2006 303 309
K. Bantubungi C. Jacquard A. Greco A. Pintor A. Chtarto K. Tai M.C. Galas L. Tenenbaum N. Deglon P. Popoli L. Minghetti E. Brouillet J. Brotchi M. Levivier S.N. Schiffmann D. Blum Minocycline in phenotypic models of Huntington's disease Neurobiol. Dis. 18 2005 206 217
M.F. Beal N.W. Kowall D.W. Ellison M.F. Mazurek K.J. Swartz J.B. Martin Replication of the neurochemical characteristics of Huntington's disease by quinolinic acid Nature 321 1986 168 171
A. Belmadani P.B. Tran D. Ren R.J. Miller Chemokines regulate the migration of neural progenitors to sites of neuroinflammation J. Neurosci. 26 2006 3182 3191
J.C. Bensadoun L.P. de Almeida M. Dreano P. Aebischer N. Deglon Neuroprotective effect of interleukin-6 and IL6/IL6R chimera in the quinolinic acid rat model of Huntington's syndrome Eur. J. Neurosci. 14 2001 1753 1761
N. Bizat J.M. Hermel F. Boyer C. Jacquard C. Creminon S. Ouary C. Escartin P. Hantraye S. Kajewski E. Brouillet Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: implications for Huntington's disease J. Neurosci. 23 2003 5020 5030
A. Bjorklund U. Stenevi Intracerebral neural implants: neuronal replacement and reconstruction of damaged circuitries Annu. Rev. Neurosci. 7 1984 279 308
D. Blum D. Gall M.C. Galas P. d'Alcantara K. Bantubungi S.N. Schiffmann The adenosine A1 receptor agonist adenosine amine congener exerts a neuroprotective effect against the development of striatal lesions and motor impairments in the 3-nitropropionic acid model of neurotoxicity J. Neurosci. 22 2002 9122 9133
D. Blum R. Hourez M.C. Galas P. Popoli S.N. Schiffmann Adenosine receptors and Huntington's disease: implications for pathogenesis and therapeutics Lancet Neurol. 2 2003 366 374
M. Bosch J.R. Pineda C. Sunol J. Petriz E. Cattaneo J. Alberch J.M. Canals Induction of GABAergic phenotype in a neural stem cell line for transplantation in an excitotoxic model of Huntington's disease Exp. Neurol. 190 2004 42 58
J.P. Brown S. Couillard-Despres C.M. Cooper-Kuhn J. Winkler L. Aigner H.G. Kuhn Transient expression of doublecortin during adult neurogenesis J. Comp. Neurol. 467 2003 1 10
P.G. Clarke How inaccurate is the Abercrombie correction factor for cell counts? Trends Neurosci. 15 1992 211 212
T. Collin A. Arvidsson Z. Kokaia O. Lindvall Quantitative analysis of the generation of different striatal neuronal subtypes in the adult brain following excitotoxic injury Exp. Neurol. 195 2005 71 80
O. Cooper O. Isacson Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons J. Neurosci. 24 2004 8924 8931
S. Couillard-Despres B. Winner S. Schaubeck R. Aigner M. Vroemen N. Weidner U. Bogdahn J. Winkler H.G. Kuhn L. Aigner Doublecortin expression levels in adult brain reflect neurogenesis Eur. J. Neurosci. 21 2005 1 14
J. Croitoru-Lamoury G.J. Guillemin D. Dormont B.J. Brew Quinolinic acid up-regulates chemokine production and chemokine receptor expression in astrocytes Adv. Exp. Med. Biol. 527 2003 37 45
M.A. Curtis E.B. Penney A.G. Pearson W.M. Roon-Mom N.J. Butterworth M. Dragunow B. Connor R.L. Faull Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain Proc. Natl. Acad. Sci. U. S. A. 100 2003 9023 9027
K.M. Dhandapani F.M. Wade C. Wakade V.B. Mahesh D.W. Brann Neuroprotection by stem cell factor in rat cortical neurons involves Akt and NF-kB J. Neurochem. 95 2005 9 19
M.A. Eglitis D. Dawson K.W. Park M.M. Mouradian Targeting of marrow-derived astrocytes to the ischemic brain Neuroreport 10 1999 1289 1292
J.G. Emsley B.D. Mitchell G. Kempermann J.D. Macklis Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells Prog. Neurobiol. 75 2005 321 341
A. Erlandsson J. Larsson K. Forsberg-Nilsson Stem cell factor is a chemoattractant and a survival factor for CNS stem cells Exp. Cell Res. 301 2004 201 210
M.C. Geloso S. Giannetti C. Cenciarelli M. Budoni P. Casalbore G. Maira F. Michetti Transplantation of foetal neural stem cells into the rat hippocampus during trimethyltin-induced neurodegeneration Neurochem. Res. 32 12 2007 2054 2061
J. Glaspy Clinical applications of stem cell factor Curr. Opin. Hematol. 3 1996 223 229
P. Guidetti R.E. Luthi-Carter S.J. Augood R. Schwarcz Neostriatal and cortical quinolinate levels are increased in early grade Huntington's disease Neurobiol. Dis. 17 2004 455 461
H.T. Hassan A. Zander Stem cell factor as a survival and growth factor in human normal and malignant hematopoiesis Acta Haematol. 95 1996 257 262
W.D. Hill D.C. Hess A. Martin-Studdard J.J. Carothers J. Zheng D. Hale M. Maeda S.C. Fagan J.E. Carroll S.J. Conway SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury J. Neuropathol. Exp. Neurol. 63 2004 84 96
J. Imitola K. Raddassi K.I. Park F.J. Mueller M. Nieto Y.D. Teng D. Frenkel J. Li R.L. Sidman C.A. Walsh E.Y. Snyder S.J. Khoury 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. U. S. A. 101 2004 18117 18122
O. Isacson The production and use of cells as therapeutic agents in neurodegenerative diseases Lancet Neurol. 2N 2003 417 424
K. Jin X.O. Mao Y. Sun L. Xie D.A. Greenberg Stem cell factor stimulates neurogenesis in vitro and in vivo J. Clin. Invest. 110 2002 311 319
K. Jin A.L. Peel X.O. Mao L. Xie B.A. Cottrell D.C. Henshall D.A. Greenberg Increased hippocampal neurogenesis in Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 101 2004 343 347
A.L. Kendall F.D. Rayment E.M. Torres H.F. Baker R.M. Ridley S.B. Dunnett Functional integration of striatal allografts in a primate model of Huntington's disease Nat. Med. 4 1998 727 729
S. Kelly T.M. Bliss A.K. Shah G.H. Sun M. Ma W.C. Foo J. Masel M.A. Yenari I.L. Weissman N. Uchida T. Palmer G.K. Steinberg Transplanted human fetal neural stem cells survive, migrate, and differentiate in ischemic rat cerebral cortex Proc. Natl. Acad. Sci. U. S. A. 101 2004 11839 11844
Z. Kokaia O. Lindvall Neurogenesis after ischaemic brain insults Curr. Opin. Neurobiol. 13 2003 127 132
J.H. Kordower E.Y. Chen C. Winkler R. Fricker V. Charles A. Messing E.J. Mufson S.C. Wong J.M. Rosenstein A. Bjorklund D.F. Emerich J. Hammang M.K. Carpenter Grafts of EGF-responsive neural stem cells derived from GFAP-hNGF transgenic mice: trophic and tropic effects in a rodent model of Huntington's disease J. Comp. Neurol. 387 1997 96 113
D.A. Lim G.J. Fishell A. Alvarez-Buylla Postnatal mouse subventricular zone neuronal precursors can migrate and differentiate within multiple levels of the developing neuraxis Proc. Natl. Acad. Sci. U. S. A. 94 1997 14832 14836
O. Lindvall Z. Kokaia A. Martinez-Serrano Stem cell therapy for human neurodegenerative disorders—how to make it work Nat. Med. 10 2004 S42 S50
D. Linnekin Early signaling pathways activated by c-Kit in hematopoietic cells Int. J. Biochem. Cell Biol. 31 1999 1053 1074
A. Mahmood D. Lu L. Wang Y. Li M. Lu M. Chopp Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells Neurosurgery 49 2001 1196 1203
A. Martinez-Serrano A. Bjorklund Protection of the neostriatum against excitotoxic damage by neurotrophin-producing, genetically modified neural stem cells J. Neurosci. 16 1996 4604 4616
Y. Matsui K.M. Zsebo B.L. Hogan Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit Nature 347 1990 667 669
J.L. McBride S.P. Behrstock E.Y. Chen R.J. Jakel I. Siegel C.N. Svendsen J.H. Kordower Human neural stem cell transplants improve motor function in a rat model of Huntington's disease J. Comp. Neurol. 475 2004 211 219
M. Modo R.P. Stroemer E. Tang S. Patel H. Hodges Effects of implantation site of stem cell grafts on behavioral recovery from stroke damage Stroke 33 2002 2270 2278
N. Nakao T. Itakura Fetal tissue transplants in animal models of Huntington's disease: the effects on damaged neuronal circuitry and behavioral deficits Prog. Neurobiol. 61 2000 313 338
H. Nishino H. Hida N. Takei M. Kumazaki K. Nakajima H. Baba Mesencephalic neural stem (progenitor) cells develop to dopaminergic neurons more strongly in dopamine-depleted striatum than in intact striatum Exp. Neurol. 164 2000 209 214
H. Ohta A. Tohda Y. Nishimune Proliferation and differentiation of spermatogonial stem cells in the w/wv mutant mouse testis Biol. Reprod. 69 2003 1815 1821
S. Palfi F. Conde D. Riche E. Brouillet C. Dautry V. Mittoux A. Chibois M. Peschanski P. Hantraye Fetal striatal allografts reverse cognitive deficits in a primate model of Huntington disease Nat. Med. 4 1998 963 966
M. Peschanski A.C. Bachoud-Levi P. Hantraye Integrating fetal neural transplants into a therapeutic strategy: the example of Huntington's disease Brain 127 2004 1219 1228
B.A. Reynolds S. Weiss Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1992 1707 1710
P. Rieske A. Azizi B. Augelli J. Gaughan B. Krynska A population of human brain parenchymal cells express markers of glial, neuronal and early neural cells and differentiate into cells of neuronal and glial lineages Eur. J. Neurosci. 25 2007 31 37
J.K. Ryu J. Kim S.J. Cho K. Hatori A. Nagai H.B. Choi M.C. Lee J.G. McLarnon S.U. Kim Proactive transplantation of human neural stem cells prevents degeneration of striatal neurons in a rat model of Huntington disease Neurobiol. Dis. 16 2004 68 77
C. Sotelo R.M. Alvarado-Mallart Reconstruction of the defective cerebellar circuitry in adult Purkinje cell degeneration mutant mice by Purkinje cell replacement through transplantation of solid embryonic implants Neuroscience 20 1987 1 22
L. Sun J. Lee H.A. Fine Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury J. Clin. Invest. 113 2004 1364 1374
Y.T. Tai C.N. Svendsen Stem cells as a potential treatment of neurological disorders Curr. Opin. Pharmacol. 4 2004 98 104
A.S. Tattersfield R.J. Croon Y.W. Liu A.P. Kells R.L. Faull B. Connor Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease Neuroscience 127 2004 319 332
E. Wandzioch C.E. Edling R.H. Palmer L. Carlsson B. Hallberg Activation of the MAP kinase pathway by c-Kit is PI-3 kinase dependent in hematopoietic progenitor/stem cell lines Blood 104 2004 51 57
C. Watts S.B. Dunnett Effects of severity of host striatal damage on the morphological development of intrastriatal transplants in a rodent model of Huntington's disease: implications for timing of surgical intervention J. Neurosurg. 89 1998 267 274
H. Wichterle J.M. Garcia-Verdugo D.G. Herrera A. Alvarez-Buylla Young neurons from medial ganglionic eminence disperse in adult and embryonic brain Nat. Neurosci. 2 1999 461 466
D.E. Williams S.D. Lyman Characterization of the gene-product of the Steel locus Prog. Growth Factor Res. 3 1991 235 242
S. Wislet-Gendebien G. Hans P. Leprince J.M. Rigo G. Moonen B. Rogister Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype Stem Cells 23 2005 392 402
S. Wislet-Gendebien P. Leprince G. Moonen B. Rogister Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells J. Cell Sci. 116 2003 3295 3302
