Histological findings on fetal striatal grafts in a Huntington's disease patient early after transplantation

Neuroscience

Volumn 160, Issue 3, 2009, Pages 661-675

  Capetian, P ^a   Knoth, R ^a   Maciaczyk, J ^a   Pantazis, G ^c   Ditter, M ^a   Bokla, L ^a   Landwehrmeyer, G B ^b   Volk, B ^a   Nikkhah, G ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY HOSPITAL ULM   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

cell transplantation; development; fetal tissue; Huntington's disease

Indexed keywords

CALRETININ; CELL NUCLEUS ANTIGEN; DOPAMINE RECEPTOR; PHOSPHOPROTEIN DARPP 32; SOMATOSTATIN; TYROSINE 3 MONOOXYGENASE;

ADULT; ARTICLE; ASTROCYTE; CASE REPORT; CELL DEGENERATION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; CLINICAL ASSESSMENT; CLINICAL FEATURE; COMPREHENSION; ELECTRIC POTENTIAL; HOST CELL; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INTERNEURON; MALE; MENTAL FUNCTION; MIGRATION; MITOSIS RATE; NERVE CELL; NEUROEPITHELIUM; PATIENT SATISFACTION; PHENOTYPE; PRIORITY JOURNAL; STRIATE CORTEX; TREATMENT DURATION;

ADULT; ASTROCYTES; BRAIN TISSUE TRANSPLANTATION; CAUDATE NUCLEUS; CELL LINEAGE; CELL MOVEMENT; CORPUS STRIATUM; FATAL OUTCOME; FETAL TISSUE TRANSPLANTATION; HUMANS; HUNTINGTON DISEASE; INTERNEURONS; MALE; MITOSIS; NEUROEPITHELIAL CELLS; NEURONS; PHENOTYPE; PUTAMEN;

EID: 64449085619     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.02.035     Document Type: Article

References (56)

1. Bachoud-Levi A.C., Gaura V., Brugieres P., Lefaucheur J.P., Boisse M.F., Maison P., Baudic S., Ribeiro M.J., Bourdet C., Remy P., Cesaro P., Hantraye P., and Peschanski M. 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
2. Bachoud-Levi A.C., Remy P., Nguyen J.P., Brugieres P., Lefaucheur J.P., Bourdet C., Baudic S., Gaura V., Maison P., Haddad B., Boisse M.F., Grandmougin T., Jeny R., Bartolomeo P., Dalla Barba G., Degos J.D., Lisovoski F., Ergis A.M., Pailhous E., Cesaro P., Hantraye P., and Peschanski M. Motor and cognitive improvements in patients with Huntington's disease after neural transplantation. Lancet 356 (2000) 1975-1979
3. Bakay R.A., Boyer K.L., Freed C.R., and Ansari A.A. Immunological responses to injury and grafting in the central nervous system of nonhuman primates. Cell Transplant 7 (1998) 109-120
4. Baker-Cairns B.J., Sloan D.J., Broadwell R.D., Puklavec M., and Charlton H.M. Contributions of donor and host blood vessels in CNS allografts. Exp Neurol 142 (1996) 36-46
5. Bancroft J.D., and Gamble M. Theory and practice of histological techniques (2002), Churchill Livingstone, Orlando, FL 375-376
6. Barker R.A., and Widner H. Immune problems in central nervous system cell therapy. NeuroRx 1 (2004) 472-481
7. Bates. Huntington's disease. GPMK (2002), Oxford University Press, Oxford, UK
8. Batista C.M., Kippin T.E., Willaime-Morawek S., Shimabukuro M.K., Akamatsu W., and van der Kooy D. A progressive and cell non-autonomous increase in striatal neural stem cells in the Huntington's disease R6/2 mouse. J Neurosci 26 (2006) 10452-10460
9. Bedard A., Gravel C., and Parent A. Chemical characterization of newly generated neurons in the striatum of adult primates. Exp Brain Res Exp Hirnforschung 170 (2006) 501-512
10. Boer G.J. Ethical guidelines for the use of human embryonic or fetal tissue for experimental and clinical neurotransplantation and research. Network of European CNS Transplantation and Restoration (NECTAR). J Neurol 242 (1994) 1-13
11. Broadwell R.D., Baker B.J., Ebert P.S., and Hickey W.F. Allografts of CNS tissue possess a blood-brain barrier: III. Neuropathological, methodological, and immunological considerations. Microsc Res Tech 27 (1994) 471-494
12. Cossette M., Lecomte F., and Parent A. Morphology and distribution of dopaminergic neurons intrinsic to the human striatum. J Chem Neuroanat 29 (2005) 1-11
13. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., and Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 (2005) 1-14
14. Curtis M.A., Penney E.B., Pearson J., Dragunow M., Connor B., and Faull R.L. The distribution of progenitor cells in the subependymal layer of the lateral ventricle in the normal and Huntington's disease human brain. Neuroscience 132 (2005) 777-788
15. D'Amour K.A., and Gage F.H. Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc Natl Acad Sci U S A 100 Suppl 1 (2003) 11866-11872
16. Dunnett S.B., Nathwani F., and Bjorklund A. The integration and function of striatal grafts. Prog Brain Res 127 (2000) 345-380
17. Dunnett S.B., and Rosser A.E. Cell therapy in Huntington's disease. NeuroRx 1 (2004) 394-405
18. Ellis P., Fagan B.M., Magness S.T., Hutton S., Taranova O., Hayashi S., McMahon A., Rao M., and Pevny L. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 26 (2004) 148-165
19. Freeman T.B., Cicchetti F., Hauser R.A., Deacon T.W., Li X.J., Hersch S.M., Nauert G.M., Sanberg P.R., Kordower J.H., Saporta S., and Isacson O. Transplanted fetal striatum in Huntington's disease: phenotypic development and lack of pathology. Proc Natl Acad Sci U S A 97 (2000) 13877-13882
20. Fricker-Gates R.A., White A., Gates M.A., and Dunnett S.B. Striatal neurons in striatal grafts are derived from both post-mitotic cells and dividing progenitors. Eur J Neurosci 19 (2004) 513-520
21. Gage F.H. Mammalian neural stem cells. Science 287 (2000) 1433-1438
22. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
23. Hatten M.E. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13 (1990) 179-184
24. Hauser S.L., Bhan A.K., Gilles F., Kemp M., Kerr C., and Weiner H.L. Immunohistochemical analysis of the cellular infiltrate in multiple sclerosis lesions. Ann Neurol 19 (1986) 578-587
25. Huot P., Levesque M., and Parent A. The fate of striatal dopaminergic neurons in Parkinson's disease and Huntington's chorea. Brain 130 (2007) 222-232
26. Hurelbrink C.B., Armstrong R.J., Dunnett S.B., Rosser A.E., and Barker R.A. Neural cells from primary human striatal xenografts migrate extensively in the adult rat CNS. Eur J Neurosci 15 (2002) 1255-1266
27. Hurelbrink C.B., and Barker R.A. Migration of cells from primary transplants of allo- and xenografted foetal striatal tissue in the adult rat brain. Eur J Neurosci 21 (2005) 1503-1510
28. Jimenez D., Lopez-Mascaraque L.M., Valverde F., and De Carlos J.A. Tangential migration in neocortical development. Dev Biol 244 (2002) 155-169
29. Kawaguchi Y., Wilson C.J., Augood S.J., and Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18 (1995) 527-535
30. Keene C.D., Sonnen J.A., Swanson P.D., Kopyov O., Leverenz J.B., Bird T.D., and Montine T.J. Neural transplantation in Huntington disease: long-term grafts in two patients. Neurology 68 (2007) 2093-2098
31. Kendall A.L., Rayment F.D., Torres E.M., Baker H.F., Ridley R.M., and Dunnett S.B. Functional integration of striatal allografts in a primate model of Huntington's disease. Nat Med 4 (1998) 727-729
32. Kordower J.H., Freeman T.B., Chen E.Y., Mufson E.J., Sanberg P.R., Hauser R.A., Snow B., and Olanow C.W. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Mov Disord 13 (1998) 383-393
33. Kordower J.H., Rosenstein J.M., Collier T.J., Burke M.A., Chen E.Y., Li J.M., Martel L., Levey A.E., Mufson E.J., Freeman T.B., and Olanow C.W. Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies. J Comp Neurol 370 (1996) 203-230
34. Krystkowiak P., Gaura V., Labalette M., Rialland A., Remy P., Peschanski M., and Bachoud-Levi A.C. Alloimmunisation to donor antigens and immune rejection following foetal neural grafts to the brain in Patients with Huntington's disease. PLoS ONE 2 (2007) e166
35. Lavado A., and Oliver G. Prox1 expression patterns in the developing and adult murine brain. Dev Dyn 236 (2007) 518-524
36. Lee M.K., Tuttle J.B., Rebhun L.I., Cleveland D.W., and Frankfurter A. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17 (1990) 118-132
37. Li J.Y., Englund E., Holton J.L., Soulet D., Hagell P., Lees A.J., Lashley T., Quinn N.P., Rehncrona S., Bjorklund A., Widner H., Revesz T., Lindvall O., and Brundin P. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14 5 (2008) 501-503
38. Lindsay R.M., and Raisman G. An autoradiographic study of neuronal development, vascularization and glial cell migration from hippocampal transplants labelled in intermediate explant culture. Neuroscience 12 (1984) 513-530
39. Liu F.C., and Graybiel A.M. Transient calbindin-D28k-positive systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 12 (1992) 674-690
40. Marin O., Anderson S.A., and Rubenstein J.L. Origin and molecular specification of striatal interneurons. J Neurosci 20 (2000) 6063-6076
41. Mendez I., Sanchez-Pernaute R., Cooper O., Vinuela A., Ferrari D., Bjorklund L., Dagher A., and Isacson O. Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease. Brain 128 (2005) 1498-1510
42. Mendez I., Vinuela A., Astradsson A., Mukhida K., Hallett P., Robertson H., Tierney T., Holness R., Dagher A., Trojanowski J.Q., and Isacson O. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat Med 14 5 (2008) 507-509
43. Nakao N., Grasbon-Frodl E.M., Widner H., and Brundin P. DARPP-32-rich zones in grafts of lateral ganglionic eminence govern the extent of functional recovery in skilled paw reaching in an animal model of Huntington's disease. Neuroscience 74 (1996) 959-970
44. Olsson M., Bjorklund A., and Campbell K. Early specification of striatal projection neurons and interneuronal subtypes in the lateral and medial ganglionic eminence. Neuroscience 84 (1998) 867-876
45. Palfi S., Conde F., Riche D., Brouillet E., Dautry C., Mittoux V., Chibois A., Peschanski M., and Hantraye P. Fetal striatal allografts reverse cognitive deficits in a primate model of Huntington disease. Nat Med 4 (1998) 963-966
46. Redmond Jr. D.E., Vinuela A., Kordower J.H., and Isacson O. Influence of cell preparation and target location on the behavioral recovery after striatal transplantation of fetal dopaminergic neurons in a primate model of Parkinson's disease. Neurobiol Dis 29 (2008) 103-116
47. Rosser A.E., Barker R.A., Harrower T., Watts C., Farrington M., Ho A.K., Burnstein R.M., Menon D.K., Gillard J.H., Pickard J., and Dunnett S.B. Unilateral transplantation of human primary fetal tissue in four patients with Huntington's disease: NEST-UK safety report ISRCTN no 36485475. J Neurol Neurosurg Psychiatry 73 (2002) 678-685
48. Schlosser B., Klausa G., Prime G., and Ten Bruggencate G. Postnatal development of calretinin- and parvalbumin-positive interneurons in the rat neostriatum: an immunohistochemical study. J Comp Neurol 405 (1999) 185-198
49. Siva A. Vasculitis of the nervous system. J Neurol 248 (2001) 451-468
50. Smith R., Bagga V., and Fricker-Gates R.A. Embryonic neural progenitor cells: the effects of species, region, and culture conditions on long-term proliferation and neuronal differentiation. J Hematother Stem Cell Res 12 (2003) 713-725
51. Smith R., Chung H., Rundquist S., Maat-Schieman M.L., Colgan L., Englund E., Liu Y.J., Roos R.A., Faull R.L., Brundin P., and Li J.Y. Cholinergic neuronal defect without cell loss in Huntington's disease. Hum Mol Genet 15 (2006) 3119-3131
52. Tattersfield A.S., Croon R.J., Liu Y.W., Kells A.P., Faull R.L., and Connor B. Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience 127 (2004) 319-332
53. Vignais L., Nait Oumesmar B., Mellouk F., Gout O., Labourdette G., Baron-Van Evercooren A., and Gumpel M. Transplantation of oligodendrocyte precursors in the adult demyelinated spinal cord: migration and remyelination. Int J Dev Neurosci 11 (1993) 603-612
54. Walker T.L., Yasuda T., Adams D.J., and Bartlett P.F. The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27 (2007) 3734-3742
55. Watts C., Brasted P.J., and Dunnett S.B. The morphology, integration, and functional efficacy of striatal grafts differ between cell suspensions and tissue pieces. Cell Transplant 9 (2000) 395-407
56. Watts C., McNamara I.R., and Dunnett S.B. Volume and differentiation of striatal grafts in rats: relationship to the number of cells implanted. Cell Transplant 9 (2000) 65-72