Neural transplants in patients with Huntington's disease undergo disease-like neuronal degeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 30, 2009, Pages 12483-12488

  Cicchetti, F ^a,b   Saporta, S ^c,d   Hauser, R A ^d   Parent, M ^e   Saint Pierre, M ^a   Sanberg, P R ^c   Li, X J ^f   Parker, J R ^g   Chu, Y ^h   Mufson, E J ^h   Kordower, J H ^h   Freeman, T B ^c  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d UNIVERSITY OF SOUTH FLORIDA   (United States)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f EMORY UNIVERSITY   (United States)

^g University of Louisville School of Medicine   (United States)

^h RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Excitotoxicity; Glutamate; Inflammation; Microglia; Mutant huntingtin

Indexed keywords

HUNTINGTIN;

ARTICLE; BRAIN CORTEX; CAUDATE NUCLEUS; CORPUS STRIATUM; DISEASE MARKER; ELECTRON MICROSCOPY; GRAFT SURVIVAL; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERNEURON; MICROGLIA; NERVE CELL DEGENERATION; NERVE PROJECTION; NERVE TRANSPLANTATION; PRIORITY JOURNAL; STRIATE CORTEX;

ANTIGENS, CD4; ANTIGENS, CD8; AUTOPSY; CORPUS STRIATUM; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; GRAFT SURVIVAL; HUMANS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; MIDDLE AGED; NERVE DEGENERATION; NEURONS; SYNAPTOPHYSIN; UBIQUITIN;

EID: 68149168120     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0904239106     Document Type: Article

References (53)

1. Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983.
2. Freeman TB, Hauser RA, Sanberg PR, Saporta S (2000) Neural transplantation for the treatment of Huntington's disease. Prog Brain Res 127:405-411.
3. Freeman TB, et al. (2000) Transplantation of human fetal striatal tissue in Huntington's disease: rationale for clinical studies. Neural transplantation in neurodegenerative disease: current status and new directions. Novartis Found Symp 231:129-144.
4. Peschanski M, Cesaro P, Hantraye P (1995) Rationale for intrastriatal grafting of striatal neuroblasts in patients with Huntington's disease. Neuroscience 68:273-285.
5. Schmidt RH, Bjorklund A, Stenevi U (1981) Intracerebral grafting of dissociated CNS tissue suspensions: a new approach for neuronal transplantation to deep brain sites. Brain Res 218:347-356.
6. Deckel AW, Robinson RG, Coyle JT, Sanberg PR (1983) Reversal of long-term locomotor abnormalities in the kainic acid model of Huntington's disease by day 18 fetal striatal implants. Eur J Pharmacol 93:287-288.
7. Isacson O, Brundin P, Kelly PA, Gage FH, Bjorklund A (1984) Functional neuronal replacement by grafted striatal neurones in the ibotenic acid-lesioned rat striatum. Nature 311:458-460.
8. Pritzel M, Isacson O, Brundin P, Wiklund L, Bjorklund A (1986) Afferent and efferent connections of striatal grafts implanted into the ibotenic acid lesioned neostriatum in adult rats. Exp Brain Res 65:112-126.
9. Wictorin K (1992) Anatomy and connectivity of intrastriatal striatal transplants. Prog Neurobiol 38:611-639.
10. Deacon TW, Pakzaban P, Isacson O (1994) The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence. Brain Res 668:211-219.
11. Isacson O, et al. (1995) Transplanted xenogeneic neural cells in neurodegenerative disease models exhibit remarkable axonal target specificity and distinct growth patterns of glial and axonal fibres. Nat Med 1:1189-1194.
12. Wictorin K, Brundin P, Gustavii B, Lindvall O, Bjorklund A (1990) Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 347:556-558.
13. Kordower JH, et al. (1995) 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 332:1118-1124.
14. Kordower JH, et al. (1997) Fetal grafting for Parkinson's disease: expression of immune markers in two patients with functional fetal nigral implants. Cell Transplant 6:213-219.
15. Campbell K, Wictorin K, Bjorklund A (1995) Neurotransmitter-related gene expression in intrastriatal striatal transplants-I. Phenotypical characterization of striatal and non-striatal graft regions. Neuroscience 64:17-33.
16. Campbell K, Wictorin K, Bjorklund A (1995) Neurotransmitter-related gene expression in intrastriatal striatal transplants-II. Characterization of efferent projecting graft neurons. Neuroscience 64:35-47.
17. Pakzaban P, Deacon TW, Burns LH, Isacson O (1993) Increased proportion of acetylcholinesterase-rich zones and improved morphological integration in host striatum offetal grafts derived from the lateral but not the medial ganglionic eminence. Exp Brain Res 97:13-22.
18. Sirinathsinghji DJ, Heavens RP, Torres EM, Dunnett SB (1993) Cholecystokinin-dependent regulation of host dopamine inputs to striatal grafts. Neuroscience 53:651-663.
19. Norman AB, Lehman MN, Sanberg PR (1989) Functional effects of fetal striatal transplants. Brain Res Bull 22:163-172.
20. Sanberg PR, Koutouzis TK, Freeman TB, Cahill DW, Norman AB (1993) Behavioral effects of fetal neural transplants: relevance to Huntington's disease. Brain Res Bull 32:493-496.
21. Hantraye P, Riche D, Maziere M, Isacson O (1992) Intrastriatal transplantation of cross-species fetal striatal cells reduces abnormal movements in a primate model of Huntington disease. Proc Natl Acad Sci USA 89:4187-4191.
22. Isacson O, Riche D, Hantraye P, Sofroniew MV, Maziere M (1989) A primate model of Huntington's disease: cross-species implantation of striatal precursor cells to the excitotoxically lesioned baboon caudate-putamen. Exp Brain Res 75:213-220.
23. Freeman TB, Sanberg PR, Isacson O (1995) Development of the human striatum: implications for fetal striatal transplantation in the treatment of Huntington's disease. Cell Transplant 4:539-545.
24. Naimi S, Jeny R, Hantraye P, Peschanski M, Riche D (1996) Ontogeny of human striatal DARPP-32 neurons in fetuses and following xenografting to the adult rat brain. Exp Neurol 137:15-25.
25. Freeman TB, et al. (2000) Transplanted fetal striatum in Huntington's disease: phenotypic development and lack of pathology. Proc Natl Acad Sci USA 97:13877-13882.
26. Freeman TB, et al. (1998) Human Fetal Tissue Transplantation for the Treatment of Movement Disorders. (AANS Publications Committee, New York) pp 177-192.
27. Brundin P, Fricker RA, Nakao N (1996) Paucity of P-zones in striatal grafts prohibit commencement of clinical trials in Huntington's disease. Neuroscience 71:895-897.
28. Nakao N, Grasbon-Frodl EM, Widner H, Brundin P (1996) 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 74:959-970.
29. Peschanski M, Cesaro P, Hantraye P (1996) What is needed versus what would be interesting to know before undertaking neural transplantation in patients with Huntington's disease. Neuroscience 71:899-900.
30. Bachoud-Levi A, et al. (2000) Safety and tolerability assessment of intrastriatal neural allografts in five patients with Huntington's disease. Exp Neurol 161:194-202.
31. Bachoud-Levi AC, et al. (2006) Effect of fetal neural transplants in patients with Huntington's disease 6 years after surgery: a long-term follow-up study. Lancet Neurol 5:303-309.
32. Hauser RA, Sandberg PR, Freeman TB, Stoessl AJ (2002) Bilateral human fetal striatal transplantation in Huntington's disease. Neurology 58:1704, author reply 1704.
33. Reuter I, et al. (2008) Long-term clinical and positron emission tomography outcome of fetal striatal transplantation in Huntington's disease. J Neurol Neurosurg Psychiatry 79:948-951.
34. Kopyov OV, Jacques S, Lieberman A, Duma CM, Eagle KS (1998) Safety of intrastriatal neurotransplantation for Huntington's disease patients. Exp Neurol 149:97-108.
35. Watts C, Dunnett SB (2000) Towards a protocol for the preparation and delivery of striatal tissue for clinical trials of transplantation in Huntington's disease. Cell Transplant 9:223-234.
36. Keene CD, et al. (2007) Neural transplantation in Huntington disease: long-term grafts in two patients. Neurology 68:2093-2098.
37. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14:504-506.
38. Kordower JH, Olanow CW, Hauser R, Chu Y, Freeman TB (2008) Transplanted dopaminergic neurons develop PD pathologic changes: A second case report. Movement Disorders 23:2303-2306.
39. Li JY, et al. (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14:501-503.
40. Vonsattel JP, et al. (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
41. Henley SM, et al. (2006) Increased rate of whole-brain atrophy over 6 months in early Huntington disease. Neurology 67:694-696.
42. Mann DM, Oliver R, Snowden JS (1993) The topographic distribution of brain atrophy in Huntington's disease and progressive supranuclear palsy. Acta Neuropathol 85:553-559.
43. Raju DV, Smith Y (2005) Differential Localization of Vesicular Glutamate Transporters 1 and 2 in the Rat Striatum. (Springer Science and Business Media, New York) pp. 601-610.
44. Biber K, Neumann H, Inoue K, Boddeke HW (2007) Neuronal "On" and "Off" signals control microglia. Trends Neurosci 30:596-602.
45. Conforti L, Adalbert R, Coleman MP (2007) Neuronal death: where does the end begin? Trends Neurosci 30:159-166.
46. Flott-Rahmel B, et al. (1997) Nerve cell lesions caused by 3-hydroxyglutaric acid: a possible mechanism for neurodegeneration in glutaric acidaemia I. J Inherit Metab Dis 20:387-390.
47. Funk CB, et al. (2005) Neuropathological, biochemical and molecular findings in a glutaric acidemia type 1 cohort. Brain 128:711-722.
48. Fusco FR, et al. (1999) Cellular localization of huntingtin in striatal and cortical neurons in rats: lack of correlation with neuronal vulnerability in Huntington's disease. J Neurosci 19:1189-1202.
49. Canals JM, et al. (2001) Expression of brain-derived neurotrophic factor in cortical neurons is regulated by striatal target area. J Neurosci 21:117-124.
50. Redmond DJ, Vinuela A, Kordower J, Isacson O (2008) 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 29:103-116.
51. Stack EC, et al. (2007) Neuroprotective effects of synaptic modulation in Huntington's disease R6/2 mice. J Neurosci 27:12908-12915.
52. Parent M, Descarries L (2008) Acetylcholine innervation of the adult rat thalamus: distribution and ultrastructural features in dorsolateral geniculate, parafascicular, and reticular thalamic nuclei. J Comp Neurol 511:678-691.
53. Capetian P, et al. (2009) Histological findings on fetal striatal grafts in a Huntington's disease patient early after transplantation. Neuroscience 160:661-675.