Long distance selective fiber outgrowth of transplanted hNT neurons in white matter tracts of the adult rat brain

Journal of Comparative Neurology

Volumn 486, Issue 4, 2005, Pages 318-330

  Baker, K Adam ^a,b   Mendez, Ivar ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b Kentucky Spinal Cord Injury Center   (United States)

Author keywords

6 hydroxydopamine; Axonal outgrowth; NT2N cells; Transplantation; Xenograft

Indexed keywords

DOPAMINE; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CORPUS CALLOSUM; CORPUS STRIATUM; FEMALE; HUMAN; HUMAN CELL; MEDIAL LEMNISCUS; NERVE ENDING; NERVE FIBER GROWTH; NERVE TRANSPLANTATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OPTIC TRACT; PARKINSONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TERATOCARCINOMA; WHITE MATTER;

ADRENERGIC AGENTS; AMPHETAMINE; ANIMALS; AXONS; BEHAVIOR, ANIMAL; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL TRANSPLANTATION; CORPUS STRIATUM; CYCLOSPORINE; FEMALE; FUNCTIONAL LATERALITY; GRAFT SURVIVAL; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MOTOR ACTIVITY; NERVE FIBERS; NEURAL PATHWAYS; NEURITES; NEURONS; OXIDOPAMINE; PHOSPHOPYRUVATE HYDRATASE; RANDOM ALLOCATION; RATS; RATS, WISTAR; ROTAROD PERFORMANCE TEST; SUBSTANTIA NIGRA; TERATOCARCINOMA; TRANSPLANTATION, HETEROLOGOUS; TYROSINE 3-MONOOXYGENASE;

EID: 18044375787     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20477     Document Type: Article

References (88)

1. Aguayo AJ, Björklund A, Stenevi U, Carlstedt T. 1984. Fetal mesencephalic neurons survive and extend long axons across peripheral nervous system grafts inserted into the adult rat striatum. Neurosci Lett 45:53-58.
2. Andrews PW. 1984. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103:285-293.
3. Andrews PW. 1987. Human teratocarcinoma stem cells: glycolipid antigen expression and modulation during differentiation. J Cell Biochem 35:321-332.
4. Armstrong RJ, Hurelbrink CB, Tyers P, Ratcliffe EL, Richards A, Dunnett SB, Rosser AE, Barker RA. 2002. The potential for circuit reconstruction by expanded neural precursor cells explored through porcine xenografts in a rat model of Parkinson's disease. Exp Neurol 175:98-111.
5. Baker KA, Hong M, Sadi D, Mendez I. 2000a. Intrastriatal and intranigral grafting of hNT neurons in the 6-OHDA rat model of Parkinson's disease. Exp Neurol 162:350-360.
6. Baker KA, Sadi D, Hong M, Mendez I, 2000b. Simultaneous intrastriatal and intranigral dopaminergic grafts in the parkinsonian rat model: role of the intranigral graft. J Comp Neurol 426:106-116.
7. Belkin AM, Stepp MA. 2000. Integrins as receptors for laminins. Microsc Res Tech 51:280-301.
8. Bignami A, Perides G, Rahemtulla F. 1993. Versican, a hyaluronate-binding proteoglycan on embryonal precartilaginous mesenchyma, is mainly expressed postnatally in rat brain. J Neurosci Res 34:97-106.
9. Björklund A, Dunnett SB, Stenevi U, Lewis ME, Iversen SD. 1980. Reinnervation of the denervated striatum by substantia nigra transplants: functional consequences as revealed by pharmacological and sensorimotor testing. Brain Res 199:307-333.
10. Björklund A, Stenevi U, Schmidt RH, Dunnett SB, Gage FH. 1983. Intracerebral grafting of neuronal cell suspensions. II. Survival and growth of nigral cell suspensions implanted in different brain sites. Acta Physiol Scand Suppl 522:9-18.
11. Björklund LM, Sanchez-Pernaute R, Chung S, Andersson T, Chen IY, McNaught KS, Brownell AL, Jenkins BG, Wahlestedt C, Kim KS, Isacson O. 2002. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc Natl Acad Sci U S A 99:2344-2349.
12. Borlongan CV, Saporta S, Poulos SG, Othberg A, Sanberg PR. 1998a. Viability and survival of hNT neurons determine degree of functional recovery in grafted ischemic rats. Neuroreport 9:2837-2842.
13. Borlongan CV, Tajima Y, Trojanowski JQ, Lee VM, Sanberg PR. 1998b. Cerebral ischemia and CNS transplantation: differential effects of grafted fetal rat striatal cells and human neurons derived from a clonal cell line. Neuroreport 9:3703-3709.
14. Borlongan CV, Tajima Y, Trojanowski JQ, Lee VM, Sanberg PR. 1998c. Transplantation of cryopreserved human embryonal carcinoma-derived neurons (NT2N cells) promotes functional recovery in ischemic rats. Exp Neurol 149:310-321.
15. Brecknell JE, Haque NS, Du JS, Muir EM, Fidler PS, Hlavin ML, Fawcett JW, Dunnett SB. 1996. Functional and anatomical reconstruction of the 6-hydroxydopamine lesioned nigrostriatal system of the adult rat. Neuroscience 71:913-925.
16. Christie SD, Sadi D, Mendez I. 2004. Intraspinal transplantation of hNT neurons in the lesioned adult rat spinal cord. Can J Neurol Sci 31:87-96.
17. Condic ML, Snow DM, Letourneau PC. 1999. Embryonic neurons adapt to the inhibitory proteoglycan aggrecan by increasing integrin expression. J Neurosci 19:10036-10043.
18. Deacon TW, Pakzaban P, Burns LH, Dinsmore J, Isacson O. 1994. Cyto-architectonic development, axon-glia relationships, and long distance axon growth of porcine striatal xenografts in rats. Exp Neurol 130:151-167.
19. Deacon T, Schumacher J, Dinsmore J, Thomas C, Palmer P, Kott S, Edge A, Penney D, Kassissieh S, Dempsey P, Isacson O. 1997. Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nat Med 3:350-353.
20. Dunnett SB, Björklund A, Stenevi U, Iversen SD. 1981. Behavioural recovery following transplantation of substantia nigra in rats subjected to 6-OHDA lesions of the nigrostriatal pathway. I. Unilateral lesions. Brain Res 215:147-161.
21. Dunnett SB, Björklund A, Schmidt RH, Stenevi U, Iversen SD. 1983. Intracerebral grafting of neuronal cell suspensions. IV. Behavioural recovery in rats with unilateral 6-OHDA lesions following implantation of nigral cell suspensions in different forebrain sites. Acta Physiol Scand Suppl 522:29-37.
22. Dunnett SB, Rogers DC, Richards SJ. 1989. Nigrostriatal reconstruction after 6-OHDA lesions in rats: combination of dopamine-rich nigral grafts and nigrostriatal 'bridge' grafts. Exp Brain Res 75:523-535.
23. Dziewczapolski G, Lie DC, Ray J, Gage FH, Schults CW. 2003. Survival and differentiation of adult rat-derived neural progenitor cells transplanted to the striatum of hemiparkinsonian rats. Exp Neurol 183:653-664.
24. Ferrari A, Ehler E, Nitsch RM, Götz J. 2000. Immature human NT2 cells grafted into mouse brain differentiate into neuronal and glial cell types. FEBS Lett 486:121-125.
25. Filbin MT. 2003. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat Rev Neurosci 4:703-713.
26. Fink JS, Schumacher JM, Ellias SL, Palmer EP, Saint-Hilaire M, Shannon K, Penn R, Starr P, VanHorne C, Kott HS, Dempsey PK, Fischman AJ, Raineri R, Manhart C, Dinsmore J, Isacson O. 2000. Porcine xenografts in Parkinson's disease and Huntington's disease patients: preliminary results. Cell Transplant 9:273-278.
27. Freed CR, Greene PE, Breeze RE, Tsai WY, DuMouchel W, Kao R, Dillon S, Winfield H, Culver S, Trojanowski JQ, Eidelberg D, Fahn S. 2001. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 344:710-719.
28. Fricker-Gates RA, Muir JA, Dunnett SB. 2004. Transplanted hNT cells ("LBS neurons") in a rat model of Huntington's disease: good survival, incomplete differentiation, and limited functional recovery. Cell Transplant 13:123-136.
29. Fu E, Nieh S, Chang HL, Wang SL. 1995. Dose-dependent gingival overgrowth induced by cyclosporin in rats. J Periodontol 66:594-598.
30. Fu E, Nieh S, Wikesjo UM, Lin FG, Shen EC. 1997. Gingival overgrowth and dental alveolar alterations: possible mechanisms of cyclosporin-induced tooth migration. An experimental study in the rat. J Periodontol 68:1231-1236.
31. Gage FH, Stenevi U, Carlstedt T, Foster G, Björklund A, Aguayo AJ. 1985. Anatomical and functional consequences of grafting mesencephalic neurons into a peripheral nerve "bridge" connected to the denervated striatum. Exp Brain Res 60:584-589.
32. Garbuzova-Davis S, Willing AE, Milliken M, Saporta S, Zigova T, Cahill DW, Sanberg PR. 2002. Positive effect of transplantation of hNT neurons (NTera 2/D1 cell-line) in a model of familial amyotrophic lateral sclerosis. Exp Neurol 174:169-180.
33. Gates MA, Thomas LB, Howard EM, Laywell ED, Sajin B, Faissner A, Götz B, Silver J, Steindler DA. 1995. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol 361:249-266.
34. Grados-Munro EM, Fournier AE. 2003. Myelin-associated inhibitors of axon regeneration. J Neurosci Res 74:479-485.
35. Guillemain I, Alonso G, Patey G, Privat A, Chaudieu I. 2000. Human NT2 neurons express a large variety of neurotransmission phenotypes in vitro. J Comp Neurol 422:380-395.
36. Hagihara K, Miura R, Kosaki R, Berglund E, Ranscht B, Yamaguchi Y. 1999. Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggests a physiological role for the interaction in the adult brain. J Comp Neurol 410:256-264.
37. Hartley RS, Trojanowski JQ, Lee VM. 1999. Differential effects of spinal cord gray and white matter on process outgrowth from grafted human NTERA2 neurons (NT2N, hNT). J Comp Neurol 415:404-418.
38. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. 2003. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509-563.
39. Hurlbert MS, Gianani RI, Hutt C, Freed CR, Kaddis FG. 1999. Neural transplantation of hNT neurons for Huntington's disease. Cell Transplant 8:143-151.
40. Isacson O, Deacon TW, Pakzaban P, Galpern WR, Dinsmore J, Burns LH. 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.
41. Jaworski DM, Fager N. 2000. Regulation of tissue inhibitor of metalloproteinase-3 (Timp-3) mRNA expression during rat CNS development. J Neurosci Res 61:396-408.
42. Johnston RE, Becker JB. 1999. Behavioral changes associated with grafts of embryonic ventral mesencephalon tissue into the striatum and/or substantia nigra in a rat model of Parkinson's disease. Behav Brain Res 104:179-187.
43. Jones LL, Sajed D, Tuszynski MH. 2003. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci 23:9276-9288.
44. Kleppner SR, Robinson KA, Trojanowski JQ, Lee VM-Y. 1995. Transplanted human neurons derived from a teratocarcinoma cell line (NTera-2) mature, integrate and survive for over 1 year in the nude mouse brain. J Comp Neurol 357:618-632.
45. Kondziolka D, Wechsler L, Goldstein S, Meltzer C, Thulborn KR, Gebel J, Jannetta P, DeCesare S, Elder EM, McGrogan M, Reitman MA, Bynum L. 2000. Transplantation of cultured human neuronal cells for patients with stroke. Neurology 55:565-569.
46. Lee VM, Andrews PW. 1986. Differentiation of NTERA-2 clonal human embryonal carcinoma cells into neurons involves the induction of all three neurofilament proteins. J Neurosci 6:514-521.
47. Lee VM, Hartley RS, Trojanowski JQ. 2000. Neurobiology of human neurons (NT2N) grafted into mouse spinal cord: implications for improving therapy of spinal cord injury. Prog Brain Res 128:299-307.
48. McGee AW, Strittmatter SM. 2003. The Nogo-66 receptor: focusing myelin inhibition of axonal regeneration. Trends Neurosci 26:193-198.
49. Meltzer CC, Kondziolka D, Villemagne VL, Weschler L, Goldstein S, Thulborn KR, Gebel J, Elder EM, DeCesare S, Jacobs A. 2001. Serial [F-18]fluorodeoxyglucose positron emission tomography after human neuronal implantation for stroke. Neurosurgery 49:586-591.
50. Mendez I, Sadi D, Hong M. 1996. Reconstruction of the nigrostriatal pathway by simultaneous intrastriatal and intranigral dopaminergic transplants. J Neurosci 16:7216-7227.
51. Mendez I, Dagher A, Hong M, Gaudet P, Weerasinghe S, McAlister V, King D, Desrosiers J, Darvesh S, Acorn T, Robertson H. 2002. Simultaneous intrastriatal and intranigral fetal dopaminergic grafts in patients with Parkinson disease: a pilot study. Report of three cases. J Neurosurg 96:589-596.
52. Milner R, Campbell IL. 2002. The integrin family of cell adhesion molecules has multiple functions within the CNS. J Neurosci Res 69:286-291.
53. Mitchell BD, Cauller LJ. 2001. Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats. Brain Res 921:68-77.
54. Miyazono M, Lee VM-Y, Trojanowski JQ. 1995. Proliferation, cell death, and neuronal differentiation in transplanted human embryonal (NTera2) cells depend on the graft site in nude and severe combined immunodeficient mice. Lab Invest 73:273-283.
55. Miyazono M, Nowell PC, Finan JL, Lee VM, Trojanowski JQ. 1996. Long-term integration and neuronal differentiation of human embryonal carcinoma cells (NTera-2) transplanted into the caudoputamen of nude mice. J Comp Neurol 376:603-613.
56. Muir JK, Raghupathi R, Saatman KE, Wilson CA, Lee VM, Trojanowski JQ, Philips MF, McIntosh TK. 1999. Terminally differentiated human neurons survive and integrate following transplantation into the traumatically injured rat brain. J Neurotrauma 16:403-414.
57. Mukhida K, Baker KA, Sadi D, Mendez I. 2001. Enhancement of sensorimotor behavioral recovery in hemiparkinsonian rats with intrastriatal, intranigral, and intrasubthalamic nucleus dopaminergic transplants. J Neurosci 21:3521-3530.
58. Nelson PT, Kondziolka D, Wechsler L, Goldstein S, Gebel J, DeCesare S, Elder EM, Zhang PJ, Jacobs A, McGrogan M, Lee VM, Trojanowski JQ. 2002. Clonal human (hNT) neuron grafts for stroke therapy: neuropathology in a patient 27 months after implantation. Am J Pathol 160:1201-1206.
59. Nikkhah G, Olsson M, Eberhard J, Bentlage C, Cunningham MG, Björklund A. 1994. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63:57-72.
60. Olanow CW, Goetz CG, Kordower JH, Stoessl AJ, Sossi V, Brin MF, Shannon KM, Nauert GM, Perl DP, Goldbold J, Freeman TB. 2003. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 54:403-414.
61. Philips MF, Muir JK, Saatman KE, Raghupathi R, Lee VM, Trojanowski JQ, McIntosh TK. 1999. Survival and integration of transplanted postmitotic human neurons following experimental brain injury in immunocompetent rats. J Neurosurg 90:116-124.
62. Pleasure SJ, Lee VM-Y. 1993. NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J Neurosci Res 15:585-602.
63. Pleasure SJ, Page C, Lee VM-Y. 1992. Pure, postmitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12:1802-1815.
64. Reynolds R, Hardy R. 1997. Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 47:455-470.
65. Rivas-Arancibia S, Willing AE, Zigova T, Rodriguez AI, Cahill DW, Sanberg PR. 2000. The effects of taurine on hNT neurons transplanted in adult rat striatum. Cell Transplant 9:751-758.
66. Saporta S, Borlongan CV, Sanberg PR. 1999. Neural transplantation of human neuroteratocarcinoma (hNT) neurons into ischemic rats. A quantitative dose-response analysis of cell survival and behavioral recovery. Neuroscience 91:519-525.
67. Saporta S, Willing AE, Colina LO, Zigova T, Milliken M, Daadi MM, Sanberg PR. 2000. In vitro and in vivo characterization of hNT neuron neurotransmitter phenotypes. Brain Res Bull 53:263-268.
68. Saporta S, Willing AE, Zigova T, Daadi MM, Sanberg PR. 2001. Comparison of calcium-binding proteins expressed in cultured hNT neurons and hNT neurons transplanted into the rat striatum. Exp Neurol 167:252-259.
69. Saporta S, Makoui AS, Willing AE, Daadi M, Cahill DW, Sanberg PR. 2002. Functional recovery after complete contusion injury to the spinal cord and transplantation of human neuroteratocarcinoma neurons in rats. J Neurosurg 97(Suppl):63-68.
70. Sawamoto K, Nakao N, Kakishita K, Ogawa Y, Toyama Y, Yamamoto A, Yamaguchi M, Mori K, Goldman SA, Itakura T, Okano H. 2001. Generation of dopaminergic neurons in the adult brain from mesencephalic precursor cells labeled with a nestin-GFP transgene. J Neurosci 21:3895-3903.
71. Schumacher JM, Ellias SA, Palmer EP, Kott HS, Dinsmore J, Dempsey PK, Fischman AJ, Thomas C, Feldman RG, Kassissieh S, Raineri R, Manhart C, Penney D, Fink JS, Isacson O. 2000. Transplantation of embryonic porcine mesencephalic tissue in patients with PD. Neurology 54:1042-1050.
72. Stipp CS, Hemler ME. 2000. Transmembrane-4-superfamily proteins CD151 and CD81 associate with α3β1 integrin, and selectively contribute to α3β1-dependent neurite outgrowth. J Cell Sci 113:1871-1882.
73. Svendsen CN, Caldwell MA, Shen J, ter Borg MG, Rosser AE, Tyers P, Karmiol S, Dunnett SB. 1997. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp Neurol 148:135-146.
74. Trojanowski JQ, Mantione JR, Lee JH, Seid DP, You T, Inge LJ, Lee VM-Y. 1993. Neurons derived from a human teratocarcinoma cell line establish molecular and structural polarity following transplantation into the rodent brain. Exp Neurol 122:283-294.
75. Wang Y, Tien LT, Lapchak PA, Hoffer BJ. 1996. GDNF triggers fiber outgrowth of fetal ventral mesencephalic grafts from nigra to striatum in 6-OHDA-lesioned rats. Cell Tissue Res 286:225-233.
76. Watson DJ, Longhi L, Lee EB, Fulp CT, Fujimoto S, Royo NC, Passini MA, Trojanowski JQ, Lee VM-Y, McIntosh TK, Wolfe JH. 2003. Genetically modified NT2N human neuronal cells mediate long-term gene expression as CNS grafts in vivo and improve functional cognitive outcome following experimental traumatic brain injury. J Neuropathol Exp Neurol 62:368-380.
77. Wictorin K, Brundin P, Sauer H, Lindvall O, Björklund A. 1992. Long distance directed axonal growth from human dopaminergic mesencephalic neuroblasts implanted along the nigrostriatal pathway in 6-hydroxydopamine lesioned adult rats. J Comp Neurol 323:475-494.
78. Wilby MJ, Sinclair SR, Muir EM, Zietlow R, Adcock KH, Horellou P, Rogers JH, Dunnett SB, Fawcett JW. 1999. A glial cell line-derived neurotrophic factor-secreting clone of the Schwann cell line SCTM41 enhances survival and fiber outgrowth from embryonic nigral neurons grafted to the striatum and to the lesioned substantia nigra. J Neurosci 19:2301-2312.
79. Willing AE, Garbuzova-Davis S, Saporta S, Milliken M, Cahill DW, Sanberg PR. 2001. hNT neurons delay onset of motor deficits in a model of amyotrophic lateral sclerosis. Brain Res Bull 56:525-530.
80. Willing AE, Saporta S, Lixian J, Milliken M, Poulos S, Bowersox SS, Sanberg PR. 2002a. Preliminary study of the behavioral effects of LBS-neuron implantation on seizure susceptibility following middle cerebral artery occlusion in the rats. Neurotox Res 4:111-118.
81. Willing AE, Zigova T, Milliken M, Poulos S, Saporta S, McGrogan M, Snable G, Sanberg PR. 2002b. Lithium exposure enhances survival of NT2N cells (hNT neurons) in the hemiparkinsonian rat. Eur J Neurosci 16:2271-2278.
82. Yang M, Stull ND, Berk MA, Snyder EY, Iacovitti L. 2002. Neural stem cells spontaneously express dopaminergic traits after transplantation into the intact or 6-hydroxydopamine-lesioned rat. Exp Neurol 177:50-60.
83. Zhou PC, Azmitia EC. 1988. Laminin facilitates and guides fiber growth of transplanted neurons in adult brain. J Chem Neuroanat 1:133-146.
84. Zhou FC, Chiang YH. 1995. Excitochemical-induced trophic bridging directs axonal growth of transplanted neurons to distal target. Cell Transplant 4:103-112.
85. Zhou FC, Chiang YH, Wang Y. 1996. Constructing a new nigrostriatal pathway in the Parkinsonian model with bridged neural transplantation in substantia nigra. J Neurosci 16:6965-6974.
86. Zigova T, Willing AE, Tedesco EM, Borlongan CV, Saporta S, Snable GL, Sanberg PR. 1999. Lithium chloride induces the expression of tyrosine hydroxylase in hNT neurons. Exp Neurol 57:251-258.
87. Zigova T, Barroso LF, Willing AE, Saporta S, McGrogan MP, Freeman TB, Sanberg PR. 2000a. Dopaminergic phenotype of hNT cells in vitro. Brain Res Dev Brain Res 122:87-90.
88. Zigova T, Pencea V, Sanberg PR, Luskin MB. 2000b. The properties of hNT cells following transplantation into the subventricular zone of the neonatal forebrain. Exp Neurol 163:31-38.