Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease

Brain

Volumn 128, Issue 7, 2005, Pages 1498-1510

  Mendez, Ivar ^a   Sanchez Pernaute, Rosario ^c   Cooper, Oliver ^c   Viñuela, Angel ^c   Ferrari, Daniela ^c   Björklund, Lars ^c   Dagher, Alain ^b   Isacson, Ole ^c,d  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c HARVARD UNIVERSITY   (United States)

^d MCLEAN HOSPITAL   (United States)

Author keywords

Dopamine neuron; Parkinson's disease; Transplantation

Indexed keywords

BIOLOGICAL MARKER; CALBINDIN; CD45 ANTIGEN; CD68 ANTIGEN; CYCLOSPORIN A; DOPA; FLUORODEOXYGLUCOSE F 18; GUANINE NUCLEOTIDE BINDING PROTEIN; IMMUNOSUPPRESSIVE AGENT; POTASSIUM; POTASSIUM CHANNEL; TYROSINE 3 MONOOXYGENASE; DOPAMINE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; KCNJ6 PROTEIN, MOUSE;

ADOPTIVE IMMUNOTHERAPY; ADULT; AGED; ARTICLE; AUTOPSY; BRAIN TRANSPLANTATION; CASE REPORT; CELL SUSPENSION; CELL TYPE; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; FEMALE; FETUS; FETUS (ANATOMY); HUMAN; HUMAN TISSUE; IMMUNOSUPPRESSIVE TREATMENT; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT GIRK2; MALE; MESENCEPHALON; MOTOR DYSFUNCTION; PARKINSON DISEASE; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PUTAMEN; SIDE EFFECT; SUBSTANTIA NIGRA; BRAIN LEVEL; CELL SURVIVAL; FETAL TISSUE TRANSPLANTATION; GRAFT SURVIVAL; IMMUNOHISTOCHEMISTRY; METHODOLOGY; MIDDLE AGED; NERVE CELL; PATHOLOGY; PHYSIOLOGY; SCINTISCANNING; TRANSPLANTATION;

AGED; AUTOPSY; BIOLOGICAL MARKERS; BRAIN CHEMISTRY; BRAIN TISSUE TRANSPLANTATION; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL SURVIVAL; CORPUS STRIATUM; DOPAMINE; FEMALE; FETAL TISSUE TRANSPLANTATION; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GRAFT SURVIVAL; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MIDDLE AGED; NEURONS; PARKINSON DISEASE; POSITRON-EMISSION TOMOGRAPHY; POTASSIUM CHANNELS, INWARDLY RECTIFYING; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 21944436225     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awh510     Document Type: Article

References (67)

1. Apostolides C, Sandford E, Hong M, Mendez I. Glial cell line-derived neurotrophic factor improves intrastriatal graft survival of stored dopaminergic cells. Neuroscience 1996; 83: 363-72.
2. Baker KA, Sadi D, Hong M, Mendez I. Simultaneous intrastriatal and intranigral dopaminergic grafts in the parkinsonian rat model: role of the intranigral graft. J Comp Neurol 2000; 426: 106-16.
3. Bandmann O, Marsden CD, Wood NW. Genetic aspects of Parkinson's disease. Mov Disord 1998; 13: 203-11.
4. Bayer SA, Wills KV, Triarhou LC, Verina T, Thomas JD, Ghetti B. Selective vulnerability of late-generated dopaminergic neurons of the substantia nigra in weaver mutant mice. Proc Natl Acad Sci USA 1995; 92: 9137-40.
5. Bjorklund L, Isacson O. Regulation of dopamine cell type and transmitter function in fetal and stem cell transplantation for Parkinson's disease. Prog Brain Res 2002; 138: 411-20.
6. Bjorklund A, Stenevi U, Schmidt RH, Dunnett SB, Gage FH. Intracerebral grafting of neuronal cell suspensions. I. Introduction and general methods of preparation. Acta Physiol Scand Suppl 1983; 522: 1-7.
7. Costantini LC, Isacson O. Immunophilin ligands and dopamine neurons: specific effects in culture and in vivo. In: Borlongan CV, Isacson O, Sanberg PR, editors. Immunosuppressant analogs in neuroprotection. Totowa, NJ: Humana Press; 2002. p. 49-66.
8. Costantini LC, Lin L, Isacson O. Medial fetal ventral mesencephalon: a preferred source for dopamine neuron grafts. Neuroreport 1997; 8: 2253-7.
9. Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28K) immunohistochemistry. Brain 1999; 122: 1421-36.
10. Espejo M, Cutillas B, Arenas TE, Ambrosio S. Increased survival of dopaminergic neurons in striatal grafts of fetal ventral mesencephalic cells exposed to neurotrophin-3 or glial cell line-derived neurotrophic factor. Cell Transplant 2000; 9: 45-53.
11. Fahn S, Elton RL, Members of the UPDRS Development Committee. Unified Parkinson's Disease Rating Scale. New York, NY: Macmillan; 1987.
12. Fearnley JM, Lees AJ. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991; 114: 2283-301.
13. Finsen BR, Sorensen T, Castellano B, Pedersen EB, Zimmer J. Leukocyte infiltration and glial reactions in xenografts of mouse brain tissue undergoing rejection in the adult rat brain. A light and electron microscopical immunocytochemical study. J Neuroimmunol 1991; 32: 159-83.
14. Freed CR, Breeze RE, Rosenberg NL, Schneck SA, Kriek E, Qi JX, et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 and 46 months after transplantation for Parkinson's disease. N Engl J Med 1992; 327: 1549-55.
15. Freed CR, Greene PE, Breeze RE, Tsai WY, DuMouchel W, Kao R, et al. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 2001; 344: 710-9.
16. Gaspar P, Ben Jelloun N, Febvret A. Sparing of the dopaminergic neurons containing calbindin-D28k and of the dopaminergic mesocortical projections in weaver mutant mice. Neuroscience 1994; 61: 293-305.
17. Geny C, Naimi-Sadaoui S, Jeny R, Belkadi AM, Juliano SL, Peschanski M. Long-term delayed vascularization of human neural transplants to the rat brain. J Neurosci 1994; 14: 7553-62.
18. Gerfen CR, Baimbridge KG, Miller JJ. The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc Natl Acad Sci USA 1985; 82: 8780-4.
19. Gerfen CR, Herkenham M, Thibault J. The neostriatal mosaic. II. Patch-and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 1987; 7: 3915-34.
20. German DC, Manaye KF, Sonsalla PK, Brooks BA. Midbrain dopaminergic cell loss in Parkinson's disease and MPTP-induced parkinsonism: sparing of calbindin-D28k-containing cells. Ann NY Acad Sci 1992; 648: 42-62.
21. Gibb WR. Melanin, tyrosine hydroxylase, calbindin and substance P in the human midbrain and substantia nigra in relation to nigrostriatal projections and differential neuronal susceptibility in Parkinson's disease. Brain Res 1992; 581: 283-91.
22. Granholm AC, Mott JL, Bowenkamp K, Eken S, Henry S, Hoffer BJ, et al. Glial cell line-derived neurotrophic factor improves survival of ventral mesencephalic grafts to the 6-hydroxydopamine lesioned striatum. Exp Brain Res 1997; 116: 29-38.
23. Graybiel AM, Ohta K, Roffler-Tarlov S. Patterns of cell and fiber vulnerability in the mesostriatal system of the mutant mouse weaver. I. Gradients and compartments. J Neurosci 1990; 10: 720-33.
24. Guatteo E, Fusco FR, Giacomini P, Bernardi G, Mercuri NB. The weaver mutation reverses the function of dopamine and GABA in mouse dopaminergic neurons. J Neurosci 2000; 20: 6013-20.
25. Haber SN, Kunishio K, Mizobuchi M, Lynd-Balta E. The orbital and medial prefrontal circuit through the primate basal ganglia. J Neurosci 1995; 15: 4851-67.
26. Hagell P, Schrag A, Piccini P, Jahanshahi M, Brown R, Rehncrona S, et al. Sequential bilateral transplantation in Parkinson's disease: effects of the second graft. Brain 1999; 122: 1121-32.
27. Haque NS, LeBlanc CJ, Isacson O. Differential dissection of the rat E16 ventral mesencephalon and survival and reinnervation of the 6-OHDA-lesioned striatum by a subset of aldehyde dehydrogenase-positive TH neurons. Cell Transplant 1997; 6: 239-48.
28. Hauser RA, Freeman TB, Snow BJ, Nauert M, Gauger L, Kordower JH, et al. Long-term evaluation of bilateral fetal nigral transplantation in Parkinson disease. Arch Neurol 1999; 56: 179-87.
29. Hebb AO, Hebb K, Ramachandran AC, Mendez I. Glial cell line-derived neurotrophic factor-supplemented hibernation of fetal ventral mesencephalic neurons for transplantation in Parkinson disease: long-term storage. J Neurosurg 2003; 98: 1078-83.
30. Hontanilla B, Parent A, Gimenez-Amaya JM. Parvalbumin and calbindin D-28k in the entopeduncular nucleus, subthalamic nucleus, and substantia nigra of the rat as revealed by double-immunohistochemical methods. Synapse 1997; 25: 359-67.
31. Inanobe A, Yoshimoto Y, Horio Y, Morishige KI, Hibino H, Matsumoto S, et al. Characterization of G-protein-gated K+ channels composed of Kir3.2 subunits in dopaminergic neurons of the substantia nigra. J Neurosci 1999; 19: 1006-17.
32. Isacson O, Deacon T. Specific axon guidance factors persist in the adult rat brain as demonstrated by pig neuroblasts transplanted to the rat. Neuroscience 1996; 75: 827-37.
33. Isacson O, Deacon TW. Neural transplantation studies reveal the brain's capacity for continuous reconstruction. Trends Neurosci 1997; 20: 477-82.
34. Isacson O, Deacon T, Schumacher JM. Immunobiology and neuroscience of xenotransplantation in neurological disease. In: Tuszynski MH, Kordower JH, editors. CNS regeneration: basic science and clinical advances. San Diego: Academic Press; 1998. p. 365-87.
35. Kordower JH, Freeman TB, Snow BJ, Vingerhoets FJG, Mufson EJ, Sanberg PR, et al. 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 1995; 332: 1118-24.
36. Kordower JH, Rosenstein JM, Collier TJ, Burke MA, Chen E-Y, Li JM, et al. Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies. J Comp Neurol 1996; 370: 203-30.
37. Kordower JH, Styren S, Clarke M, DeKosky ST, Olanow CW, Freeman TB. Fetal grafting for Parkinson's disease: expression of immune markers in two patients with functional fetal nigral implants. Cell Transplant 1997; 6: 213-9.
38. Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, et al. Core assessment program for intracerebral transplantations (CAPIT). Mov Disord 1992; 7: 2-13.
39. Leigh K, Elisevich K, Rogers KA. Vascularization and microvascular permeability in solid versus cell-suspension embryonic neural grafts. J Neurosurg 1994; 81: 272-83.
40. Liang CL, Sinton CM, German DC. Midbrain dopaminergic neurons in the mouse: co-localization with calbindin-D28K and calretinin. Neuroscience 1996; 75: 523-33.
41. Lindvall O, Hagell P. Clinical observations after neural transplantation in Parkinson's disease. Prog Brain Res 2000; 127: 299-320.
42. Lindvall O, Brundin P, Widner H, Rehncrona S, Gustavii B, Frackowiak R, et al. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science 1990; 247: 574-7.
43. Lindvall O, Sawle G, Widner H, Rothwell JC, Bjorklund A, Brooks D, et al. Evidence for long-term survival and function of dopaminergic grafts in progressive Parkinson's disease. Ann Neurol 1994; 35: 172-80.
44. Lynd-Balta E, Haber SN. The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum. Neuroscience 1994; 59: 625-40.
45. Marsden CD. Problems with long-term levodopa therapy for Parkinson's disease. Clin Neuropharmacol 1994; 17 Suppl 2: S32-44.
46. Mehta V, Hong M, Spears J, Mendez I. Enhancement of graft survival and sensorimotor behavioral recovery in rats undergoing transplantation with dopaminergic cells exposed to glial cell line-derived neurotrophic factor. J Neurosurg 1998; 88: 1088-95.
47. Mendez I, Dagher A, Hong M, Hebb A, Gaudet P, Law A, et al. Enhancement of survival of stored dopaminergic cells and promotion of graft survival by exposure of human fetal nigral tissue to glial cell line-derived neurotrophic factor in patients with Parkinson's disease. Report of two cases and technical considerations. J Neurosurg 2000a; 92: 863-9.
48. Mendez I, Hong M, Smith S, Dagher A, Desrosiers J. Neural transplantation cannula and microinjector system: experimental and clinical experience. Technical note. J Neurosurg 2000b; 92: 493-9.
49. Mendez I, Dagher A, Hong M, Gaudet P, Weerasinghe S, McAlister V, et al. Simultaneous intrastriatal and intranigral fetal dopaminergic grafts in patients with Parkinson disease: a pilot study. Report of three cases. J Neurosurg 2002; 96: 589-96.
50. Mukhida K, Baker KA, Sadi D, Mendez I. Enhancement of sensorimotor behavioral recovery in hemiparkinsonian rats with intrastriatal, intranigral, and intrasubthalamic nucleus dopaminergic transplants. J Neurosci 2001; 21: 3521-30.
51. Nemoto C, Hida T, Arai R. Calretinin and calbindin-D28k in dopaminergic neurons of the rat midbrain: a triple-labeling immunohistochemical study. Brain Res 1999; 846: 129-36.
52. Neuhoff H, Neu A, Liss B, Roeper J. I(h) channels contribute to the different functional properties of identified dopaminergic subpopulations in the midbrain. J Neurosci 2002; 22: 1290-302.
53. Nikkah G, Olsson M, Eberhard J, Bentlage C, Cunningham MG, Bjorklund A. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 1994; 53: 57-72.
54. Nurmi E, Ruottinen HM, Bergman J, Haaparanta M, Solin O, Sonninen P, et al. Rate of progression in Parkinson's disease: a 6-[18F]fluoro-L-dopa PET study. Mov Disord 2001; 16: 608-15.
55. O'Rahilly R, Muller F. Developmental stages in human embryos: including a revision of Streeter's horizons and a survey of the Carnegie collection. Washington DC: Carnegie Institution of Washington; 1987.
56. Olanow CW, Goetz CG, Kordower JH, Stoessl AJ, Sossi V, Brin MF, et al. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 2003; 54: 403-14.
57. Patlak CS, Blasberg, R.G. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J Cerebr Blood Flow Metab 1985; 5: 584-90.
58. Peschanski M, Isacson O. Fetal homotypic transplants in the excitotoxically neuron depleted thalamus. I. Light microscopy. J Comp Neurol 1988; 274: 449-63.
59. Peschanski M, Defer G, N'Guyen J, Ricolfi F, Monfort J, Remy P, et al. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson's disease following intrastriatal transplantation of fetal ventral mesencephalon. Brain 1994; 117: 487-99.
60. Piccini P, Brooks DJ, Bjorklund A, Gunn RN, Grasby PM, Rimoldi O, et al. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat Neurosci 1999; 2: 1137-40.
61. Piccini P, Lindvall O, Bjorklund A, Brundin P, Hagell P, Ceravolo R, et al. Delayed recovery of movement-related cortical function in Parkinson's disease after striatal dopaminergic grafts. Ann Neurol 2000; 48: 689-95.
62. Rajput AH, Fenton ME, Birdi S, Macaulay R, George D, Rozdilsky B, et al. Clinical-pathological study of levodopa complications. Mov Disord 2002; 17: 289-96.
63. Rosenblad C, Martinez-Serrano A, Bjorklund A. Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience 1996; 75: 979-85.
64. Schein J, Hunter D, Roffler-Tarlov S. Girk2 expression in the ventral midbrain, cerebellum, and olfactory bulb and its relationship to the murine mutation weaver. Dev Biol 1998; 204: 432-50.
65. Schultzberg M, Dunnett SB, Bjorklund A, Stenevi U, Hokfelt T, Dockray GJ, et al. Dopamine and cholecystokinin immunoreactive neurons in mesen-cephalic grafts reinnervating the neostriatum: evidence for selective growth regulation. Neuroscience 1984; 12: 17-32.
66. Yamada T, McGeer PL, Baimbridge KG, McGeer EG. Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K. Brain Res 1990; 526: 303-7.
67. Yurek DM, Fletcher-Turner A. GDNF partially protects grafted fetal dopaminergic neurons against 6-hydroxydopamine neurotoxicity. Brain Res 1999; 845: 21-7.