Transplantation of motoneurons derived from MASH1-transfected mouse ES cells reconstitutes neural networks and improves motor function in hemiplegic mice

Experimental Neurology

Volumn 189, Issue 2, 2004, Pages 280-292

  Ikeda, Ritsuko ^a   Kurokawa, Manae S ^a   Chiba, Shunmei ^a   Yoshikawa, Hideshi ^a   Hashimoto, Takuo ^a   Tadokoro, Mamoru ^a   Suzuki, Noboru ^a,b  

^a ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b ST MARIANNA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Brain injury; ES cells; MASH1; Motoneuron; Motor function; Recovery; Transplantation

Indexed keywords

BETA TUBULIN; GALACTOSYLCERAMIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; HELIX LOOP HELIX PROTEIN; NERVE CELL ADHESION MOLECULE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; CELL INTERACTION; CELL LINEAGE; CELL MIGRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; EXPRESSION VECTOR; FEMALE; FETUS; GENETIC TRANSFECTION; HEMIPLEGIA; IMMUNOHISTOCHEMISTRY; MOTONEURON; MOTOR CORTEX; MOTOR PERFORMANCE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE FIBER; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RECIPIENT; STEM CELL; WALKING;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN INJURIES; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; FEMALE; GRAFT SURVIVAL; HEMIPLEGIA; MICE; MOTOR CORTEX; MOTOR NEURONS; MOVEMENT DISORDERS; MULTIPOTENT STEM CELLS; NERVE NET; NEURAL CELL ADHESION MOLECULES; NEUROFILAMENT PROTEINS; RECOVERY OF FUNCTION; SYNAPTOPHYSIN; TRANSCRIPTION FACTORS; TRANSFECTION; TREATMENT OUTCOME; TUBULIN;

EID: 4544352728     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.05.040     Document Type: Article

References (53)

1. Allen G.V., Gerami D., Esser M.J. Conditioning effects of repetitive mild neurotrauma on motor function in an animal model of focal brain injury. Neuroscience. 99:2000;93-105
2. Arnhold S., Andressen C., Angelov D.N., Vajna R., Volsen S.G., Hescheler J., Addicks K. Embryonic stem-cell derived neurones express a maturation dependent pattern of voltage-gated calcium channels and calcium-binding proteins. Int. J. Dev. Neurosci. 18:2000;201-212
3. Bain G., Kitchens D., Yao M., Huettner J.E., Gottlieb D.I. Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168:1995;342-357
4. Benninger Y., Marino S., Hardegger R., Weissmann C., Aguzzi A., Brandner S. Differentiation and histological analysis of embryonic stem cell-derived neural transplants in mice. Brain Pathol. 10:2000;330-341
5. Bjorklund L.M., Sanchez-Pernaute R., Chung S., Andersson T., Chen I.Y., McNaught K.S., Brownell A.L., Jenkins B.G., Wahlestedt C., Kim K.S., Isacson O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. U. S. A. 99:2002;2344-2349
6. Blaugrund E., Pham T.D., Tennyson V.M., Lo L., Sommer L., Anderson D.J., Gershon M.D. Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers and Mash1-dependence. Development. 122:1996;309-320
7. Brüstle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., McKay R.D. Embryonic stem cell-derived glial precursors: a source of myelinating transplants. Science. 285:1999;754-756
8. Casarosa S., Fode C., Guillemot F. MASH1 regulates neurogenesis in the ventral telencephalon. Development. 126:1999;525-534
9. Chiba S., Iwasaki Y., Sekino H., Suzuki N. Transplantation of motoneuron-enriched neural cells derived from mouse embryonic stem cells improves motor function of hemiplegic mice. Cell Transplant. 12:2003;457-468
10. Chiba S., Ikeda R., Kurokawa S.M., Yoshikawa H., Takeno M., Nagafuchi H., Tadokoro M., Sekino H., Hashimoto T., Suzuki N. Anatomical and functional recovery by embryonic stem (ES) cell-derived neural tissue of a mouse model of brain damage. J. Neurol. Sci. 219:2004;107-117
11. Cook J.L., Marcheselli V., Alam J., Deininger P.L., Bazan N.G. Temporal changes in gene expression following cryogenic rat brain injury. Mol. Brain Res. 55:1998;9-19
12. Ereniev S.I., Akulinin V.A., Stepanov S.S., Semchenko V.V., Belichenko P.V. Effect of transplantation of embryonic nervous tissue on reorganization of interneuronal relationships after mechanical damage to sensorimotor cortex. Bull. Exp. Biol. Med. 131:2001;219-222
13. Farah M.H., Olson J.M., Sucic H.B., Hume R.I., Tapscott S.J., Turner D.L. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development. 127:2000;693-702
14. Fox G.B., Fan L., Levasseur R.A., Faden A.I. Sustained sensory/motor and cognitive deficits with neuronal apoptosis following controlled cortical impact brain injury in the mouse. J. Neurotrauma. 15:1998;599-614
15. Frank J.A., Miller B.R., Arbab A.S., Zywicke H.A., Jordan E.K., Lewis B.K., Bryant L.H. Jr., Bulte J.W. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology. 228:2003;480-487
16. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344:2001;710-719
17. Guan K., Chang H., Rolletschek A., Wobus A.M. Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res. 305:2001;171-176
18. Guillemot F., Lo L.C., Johnson J.E., Auerbach A., Anderson D.J., Joyner A.L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell. 75:1993;463-476
19. Hamm R.J., Pike B.R., O'Dell D.M., Lyeth B.G., Jenkins L.W. The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J. Neurotrauma. 11:1994;187-196
20. Herrera J., Yang H., Zhang S.C., Proschel C., Tresco P., Duncan I.D., Luskin M., Mayer-Proschel M. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp. Neurol. 171:2001;11-21
21. Hinds K.A., Hill J.M., Shapiro E.M., Laukkanen M.O., Silva A.C., Combs C.A., Varney T.R., Balaban R.S., Koretsky A.P., Dunbar C.E. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood. 102:2002;867-872
22. Hoehn M., Kustermann E., Blunk J., Wiedermann D., Trapp T., Wecker S., Focking M., Arnold H., Hescheler J., Fleischmann B.K., Schwindt W., Buhrle C. 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. U. S. A. 99:2002;16267-16272
23. Hof P.R., Young W.G., Bloom F.E., Belichenko P.V., Celio M.R. Mouse Brains: Comparative Cytoarchitectonic Atlas of the C57BL/6 and 129/Sv. 2000;Elsevier Science B.V. Press, Amsterdam
24. Horner P.J., Gage F.H. Regenerating the damaged central nervous system. Nature. 407:2000;963-970
25. Horton S., Meredith A., Richardson J.A., Johnson J.E. Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol. Cell Neurosci. 14:1999;355-369
26. Johnson J.E., Birren S.J., Anderson D.J. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature. 346:1990;858-861
27. Kashiwakura J.I., Suzuki N., Nagafuchi H., Takeno M., Takeba Y., Shimoyama Y., Sakane T. Txk, a nonreceptor tyrosine kinase of the Tec family, is expressed in T helper type 1 cells and regulates interferon γ production in human T lymphocytes. J. Exp. Med. 190:1999;1147-1154
28. Katano H., Masago A., Harada S., Iwata A., Yamada K. Differential induction of immediate early gene mRNAs following cryogenic and impact trauma with/without craniotomy in rats. Brain Res. 800:1998;69-77
29. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S.I., Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron. 28:2000;31-40
30. Kim J.H., Auerbach J.M., Rodriguez-Gomez J.A., Velasco I., Gavin D., Lumelsky N., Lee S.H., Nguyen J., Sanchez-Pernaute R., Bankiewicz K., McKay R. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature. 418:2002;50-56
31. Kordower J.H., Freeman T.B., Snow B.J., Vingerhoets F.J., Mufson E.J., Sanberg P.R., Hauser R.A., Smith D.A., Nauert G.M., Perl D.P., Olanow C.W. Neuropathological evidence of graft survival and striatal reinnervation after the transplantation of fetal mesencephalic tissue in a patient with Parkinson's disease. N. Engl. J. Med. 332:1995;1118-1124
32. Liu S., Qu Y., Stewart T.J., Howard M.J., Chakrabortty S., Holekamp T.F., McDonald J.W. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proc. Natl. Acad. Sci. U. S. A. 97:2000;6126-6131
33. Lo L., Sommer L., Anderson D.J. MASH1 maintains competence for BMP2-induced neuronal differentiation in post-migratory neural crest cells. Curr. Biol. 7:1997;440-450
34. Lo L., Tiveron M.C., Anderson D.J. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development. 125:1998;609-620
35. Lundberg C., Martinez-Serrano A., Cattaneo E., McKay R.D., Bjorklund A. Survival, integration, and differentiation of neural stem cell lines after transplantation to the adult rat striatum. Exp. Neurol. 145:1997;342-360
36. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 5:1999;1410-1412
37. Meierhan D., el-Ariss C., Neuenschwander M., Sieber M., Stackhouse J.F., Allemann R.K. DNA binding specificity of the basic-helix-loop-helix protein MASH-1. Biochemistry. 34:1995;11026-11036
38. Morita-Fujimura Y., Fujimura M., Kawase M., Chan P.H. Early decrease in apurinic/apyrimidinic endonuclease is followed by DNA fragmentation after cold injury-induced brain trauma in mice. Neuroscience. 93:1999;1465-1473
39. Mujtaba T., Rao M.S. Isolation of lineage-restricted neural precursors from cultured ES cells. Methods Mol. Biol. 185:2002;189-204
40. Nakamura Y., Sakakibara S., Miyata T., Ogawa M., Shimazaki T., Weiss S., Kageyama R., Okano H. The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20:2000;283-293
41. Okabe S., Forsberg-Nilsson K., Spiro A.C., Segal M., McKay R.D. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59:1996;89-102
42. Renoncourt Y., Carroll P., Filippi P., Arce V., Alonso S. Neurons derived in vitro from ES cells express homeoproteins characteristic of motoneurons and interneurons. Mech. Dev. 79:1998;185-197
43. Reubinoff B.E., Itsykson P., Turetsky T., Pera M.F., Reinhartz E., Itzik A., Ben-Hur T. Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 19:2001;1134-1140
44. Rossant J. Stem cells from the Mammalian blastocyst. Stem Cells. 19:2001;477-482
45. Rozas G., Guerra M.J., Labandeira-García J.L. An automated rotarod method for quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res. Protoc. 2:1997;75-84
46. Saporta S., Borlongan C.V., Sanberg P.R. Neural transplantation of human neuroteratocarcinoma (hNT) neurons into ischemic rats. a quantitative dose-response analysis of cell survival and behavioral recovery. Neuroscience. 91:1999;519-525
47. Sommer L., Shah N., Rao M., Anderson D.J. The cellular function of MASH1 in autonomic neurogenesis. Neuron. 15:1995;1245-1258
48. Tomita K., Moriyoshi K., Nakanishi S., Guillemot F., Kageyama R. Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J. 19:2000;5460-5472
49. Torii M., Matsuzaki F., Osumi N., Kaibuchi K., Nakamura S., Casarosa S., Guillemot F., Nakafuku M. Transcription factors MASH1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development. 126:1999;443-456
50. Tuttle R., Nakagawa Y., Johnson J.E., O'Leary D.D. Defects in thalamocortical axon pathfinding correlate with altered cell domains in MASH1-deficient mice. Development. 126:1999;1903-1916
51. Zhang L., Chen J., Li Y., Zhang Z.G., Chopp M. Quantitative measurement of motor and somatosensory impairments after mild (30 min) and severe (2 h) transient middle cerebral artery occlusion in rats. J. Neurol. Sci. 174:2000;141-146
52. Zhang S.C., Wernig M., Duncan I.D., Brustle O., Thomson J.A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19:2001;1129-1133
53. Zigova T., Pencea V., Betarbet R., Wiegand S.J., Alexander C., Bakay R.A.E., Luskin M.B. Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant. 7:1998;137-156