Intracerebral co-transplantation of liposomal tacrolimus improves xenograft survival and reduces graft rejection in the hemiparkinsonian rat

Neuroscience

Volumn 146, Issue 1, 2007, Pages 213-224

  Alemdar, A Y ^a   Sadi, D ^a   McAlister, V ^a   Mendez, I ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b QUEEN ELIZABETH II HEALTH SCIENCES CENTRE   (Canada)

Author keywords

local immunosuppression; neural transplantation; Parkinson's disease; rodent model of Parkinson's disease

Indexed keywords

LIPOSOME; RAPAMYCIN; TACROLIMUS; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL SUSPENSION; CIRCLING BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG FORMULATION; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; GRAFT REJECTION; IMMUNOHISTOCHEMISTRY; NERVE GRAFT; NEUROPROTECTION; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; XENOGRAFT;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; BEHAVIOR, ANIMAL; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; EMBRYO; FEMALE; IMMUNOSUPPRESSIVE AGENTS; LIPOSOMES; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; TACROLIMUS; TIME FACTORS; TRANSPLANTATION, HETEROLOGOUS; TYROSINE 3-MONOOXYGENASE;

EID: 34247572561     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.01.006     Document Type: Article

References (61)

1. Abraham R.T., and Wiederrecht G.J. Immunopharmacology of rapamycin. Annu Rev Immunol 14 (1996) 483-510
2. Aebischer P., Winn S.R., and Galletti P.M. Transplantation of neural tissue in polymer capsules. Brain Res 448 (1988) 364-368
3. Alemdar A.Y., Baker K.A., Sadi D., McAlister V.C., and Mendez I. Liposomal tacrolimus administered systemically and within the donor cell suspension improves xenograft survival in hemiparkinsonian rats. Exp Neurol 172 (2001) 416-424
4. Alemdar A.Y., Sadi D., McAlister V.C., and Mendez I. Liposomal formulations of tacrolimus and rapamycin increase graft survival and fiber outgrowth of dopaminergic grafts. Cell Transplant 13 (2004) 263-271
5. Avramut M., Zeevi A., and Achim C.L. The immunosuppressant drug FK506 is a potent trophic agent for human fetal neurons. Brain Res Dev Brain Res 132 (2001) 151-157
6. Baker-Cairns B.J., Sloan D.J., Broadwell R.D., Puklavec M., and Charlton H.M. Contribution of donor and host blood vessels in CNS allografts. Exp Neurol 142 (1996) 36-46
7. Berden J.H., Hoitsma A.J., Merx J.L., and Keyser A. Severe central-nervous-system toxicity associated with cyclosporine. Lancet 1 (1985) 219-220
8. Björklund A., Stenevi U., Dunnett S.B., and Gage F.H. Cross-species neural grafting in a rat model of Parkinson's disease. Nature 298 (1982) 652-654
9. Borlongan C.V., Freeman T.B., Scorcia T.A., Sherman K.A., Olanow C.W., Cahill D.W., and Sanberg P.R. CNS immunological modulation of neural graft rejection and survival. Neurol Res 18 (1996) 297-304
10. Borlongan C.V., Lind J.G., Dillon-Carter O., Yu G., Hadman M., Cheng C., Carroll J., and Hess D.C. Intracerebral xenografts of mouse bone marrow cells in adult rats facilitate restoration of cerebral blood flow and blood-brain barrier. Brain Res 1009 (2004) 26-33
11. Broadwell R.D., Charlton H.M., Ebert P., Hickey W.F., Villegas J.C., and Wolf A.L. Angiogenesis and the blood-brain barrier in solid and dissociated cell grafts within the CNS. Prog Brain Res 82 (1990) 95-101
12. Castilho R.F., Hansson O., and Brundin P. FK506 and cyclosporine A enhance the survival of cultured and grafted rat embryonic dopamine neurons. Exp Neurol 164 (2000) 94-101
13. Cho C.S., Chang Z., Elkahwaji J., Scheunemann T.L., Manthei E.R., Colburn M., Knechtle S.J., and Hamawy M.M. Rapamycin antagonizes cyclosporine A- and tacrolimus (FK506)-mediated augmentation of linker for activation of T cell expression in T cells. Int Immunol 15 (2003) 1369-1378
14. Costantini L.C., Chaturvedi P., Armistead D.M., McCaffrey P.G., Deacon T.W., and Isacson O. A novel immunophilin ligand: distinct branching effects on dopaminergic neurons in culture and neurotrophic actions after oral administration in an animal model of Parkinson's disease. Neurobiol Dis 5 (1998) 97-106
15. Costantini L.C., and Isacson O. Immunophilin ligands and GDNF enhance neurite branching or elongation from developing dopamine neurons in culture. Exp Neurol 164 (2000) 60-70
16. Date I., Shingo T., Yoshida H., Fujiwara K., Kobayashi K., and Ohmoto T. Grafting of encapsulated dopamine-secreting cells in Parkinson's disease: long-term primate study. Cell Transplant 9 (2000) 705-709
17. Deacon T., Schumacher J., Dinsmore J., Thomas C., Palmer P., Kott S., Edge A., Penney D., Kassissieh S., Dempsey P., and Isacson O. Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nat Med 3 (1997) 350-353
18. Duan W.M., Widner H., and Brundin P. Temporal pattern of host responses against intrastriatal grafts of syngeneic, allogeneic, or xenogeneic embryonic neuronal tissue in rats. Exp Brain Res 104 (1995) 227-242
19. Dumont F.J., Kastner C., Iacovone F., and Fischer P.A. Quantitative and temporal analysis of the cellular interaction of FK-506 and rapamycin in T-lymphocytes. J Pharmacol Exp Ther 268 (1994) 32-41
20. Dumont F.J., Melino M.R., Staruch M.J., Koprak S.L., Fischer P.A., and Sigal N.H. The immunosuppressive macrolides FK-506 and rapamycin act as reciprocal antagonists in murine T-cells. J Immunol 144 (1990) 1418-1424
21. Emerich D.F., Winn S.R., Christenson L., Palmatier M.A., Gentile F.T., and Sanberg P.R. A novel approach to neural transplantation in Parkinson's disease: use of polymer-encapsulated cell therapy. Neurosci Biobehav Rev 16 (1992) 437-447
22. Fink J.S., Schumacher J.M., Ellis S.L., Plamer E.P., and Saint-Hilare M. Porcine xenografts in Parkinson's and Huntington's disease patients: preliminary results. Cell Transplant 9 (2000) 273-278
23. Finsen B.R., Sorensen T., Castellano B., Pedersen E.B., and 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 32 (1991) 159-183
24. Freed C.R., Breeze R.E., Rosenberg N.L., Schneck S.A., Kriek E., Qi J.X., Lone T., Zhang Y.B., Snyder J.A., Wells T.H., et al. Survival of implanted fetal dopamine cells and neurologic improvement 12 to 46 months after transplantation for Parkinson's disease. N Engl J Med 327 (1992) 1549-1555
25. 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., and Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N Engl J Med 344 (2001) 710-719
26. Gingras A.C., Raught B., and Sonenberg N. Control of translation by the target of rapamycin proteins. Prog Mol Subcell Biol 27 (2001) 143-174
27. Gundersen H.J.G., and Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147 (1987) 229-263
28. Henderson B.T., Clough C.G., Hughes R.C., Hitchcock E.R., and Kenny B.G. Implantation of human fetal ventral mesencephalon to the right caudate nucleus in advanced Parkinson's disease. Arch Neurol 48 (1991) 822-827
29. Hitchcock E.R., Kenny B.G., Clough C.G., Hughes R.C., Henderson B.T., and Detta A. Stereotactic implantation of foetal mesencephalon (STIM): the UK experience. Prog Brain Res 82 (1990) 723-728
30. Honey C.R., Clarke D.J., Dallman M.J., and Charlton H.M. Human neural graft function in rats treated with anti-interleukin II receptor antibody. Neuroreport 1 (1990) 247-249
31. Honey C.R., Obochi M.O., Shen H., Margaron P., Yip S., and Levy J.G. Reduced xenograft rejection in rat striatum after pretransplant photodynamic therapy of murine neural xenografts. J Neurosurg 91 (2000) 127-131
32. Kino T.H., Hatanaka S., Miyata S., Inamura N., Nishiyama M., Yajima T., Goto T., Okuhara M., Kohsaka M., Aoki H., and Ochiai T. FK-506, a novel immunosuppressant isolated from a Streptomyces. II. Immunosuppressive efficacy of newly developed liposomal FK-506 in vitro. J Antibiot (Tokyo) 40 (1987) 1256-1265
33. Ko S., Nakajima Y., Kanehiro H., Yoshimura A., and Nakano H. The pharmacokinetic benefits of newly developed liposome-incorporated FK506. Transplantation 58 (1994) 1142-1144
34. Kordower J.H., Styren S., Clarke M., DeKosky S.T., Olanow C.W., and Freeman T.B. Fetal grafting for Parkinson's disease: expression of immune markers in two patients with functional fetal nigral implants. Cell Transplant 6 (1997) 213-219
35. Lopez-Lozano J.J., Bravo G., Brera B., Dargallo J., Salmean J., Uria J., Insausti J., Martinez R., Sanchez P., de la Torre C., Moreno R., and The CPH Neural Transplantation Group. Regression of parkinsonian fetal ventral mesencephalon grafts upon withdrawal of cyclosporine A immunosuppression. Transplant Proc 29 (1997) 977-980
36. Lopez-Lozano J.J., Bravo G., Brera B., Millan I., Dargallo J., Salmean J., Uria J., and Insausti J. Long-term improvement in patients with severe Parkinson's disease after implantation of fetal ventral mesencephalic tissue in a cavity of the caudate nucleus: 5-year follow up in 10 patients. J Neurosurg 86 (1997) 931-942
37. Lyons W.E., George E.B., Dawson T.M., Steiner J.P., and Snyder S.H. Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC12 cells and sensory ganglia. Proc Natl Acad Sci U S A 91 (1994) 3191-3195
38. McAlister V.C., Peltekian K.M., Malatjalian D.A., Colohan S., MacDonald S., Bitter-Suermann H., and MacDonald A.S. Orthotopic liver transplantation using low-dose tacrolimus and sirolimus. Liver Transpl 7 (2001) 701-708
39. Medawar P.B. Immunity to homologous grafted skin: III. Fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br J Exp Pathol 29 (1948) 58-69
40. Mendez I., Sanchez-Pernaute R., Cooper O., Vinuela A., Ferrari D., Björklund 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
41. Nikkhah G., Olsson M., Eberhard J., Bentlage C., Cunningham M.G., and Björklund A. A microtransplantation approach for cell suspension grafting in the rat Parkinson model: a detailed account of the methodology. Neuroscience 63 (1994) 57-72
42. Olanow C.W., Goetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., Shannon K.M., Nauert G.M., Perl D.P., Godbold J., and Freeman T.B. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann Neurol 54 (2003) 403-414
43. Pakzaban P., Deacon T.W., Burns L.H., Dinsmore J., and Isacson O. A novel mode of immunoprotection of neural xenotransplants: masking of donor major histocompatibility complex class I enhances transplant survival in the central nervous system. Neuroscience 65 (1995) 983-996
44. Parker E.M., Monopoli A., Ongini E., Lozza G., and Babij C.M. Rapamycin, but not FK-506 and GPI-1046, increases neurite outgrowth in PC12 cells by inhibiting cell cycle progression. Neuropharmacology 39 (2000) 1913-1919
45. Piccini P., Lindvall O., Björklund A., Brundin P., Hagell P., Ceravolo R., Oertel W., Quinn N., Samuel M., Rehncrona S., Widner H., and Brooks D.J. Delayed recovery of movement-related cortical function in Parkinson's disease after striatal dopaminergic grafts. Ann Neurol 48 (2000) 689-695
46. Sabatini D.M., Erdjument-Bromage H., Lui M., Tempst P., and Snyder S.H. RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78 (1994) 35-43
47. Sakai K., Date I., Yoshimoto Y., Arisawa T., Nakashima H., Furuta T., Asari S., and Ohmoto T. The effect of a new immunosuppressive agent, FK-506, on xenogeneic neural transplantation in rodents. Brain Res 565 (1991) 167-170
48. Sanberg P.R., Borlongan C.V., Saporta S., and Cameron D.F. Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain. Nat Biotechnol 14 (1996) 1692-1695
49. Saporta S., Cameron D.F., Borlongan C.V., and Sanberg P.R. Survival of rat and porcine Sertoli cell transplants in the rat striatum without cyclosporine-A immunosuppression. Exp Neurol 146 (1997) 299-304
50. Schumacher J.M., Ellias S.A., Palmer E.P., Kott H.S., Dinsmore J., Dempsey P.K., Fischman A.J., Thomas C., Feldman R.G., Kassissieh S., Raineri R., Manhart C., Penney D., Fink J.S., and Isacson O. Transplantation of embryonic porcine mesencephalic tissue in patients with PD. Neurology 54 (2000) 1042-1050
51. Selawry H.P., Kotb M., Herrod H.G., and Lu Z.N. Production of a factor, or factors, suppressing IL-2 production and T cell proliferation by Sertoli cell-enriched preparations: A potential role for islet transplantation in an immunologically privileged site. Transplantation 52 (1991) 846-850
52. Singh N., Bonham A., and Fukui M. Immunosuppressive-associated leukoencephalopathy in organ transplant recipients. Transplantation 69 (2000) 467-472
53. Small S.L., Fukui M.B., Bramblett G.T., and Eidelman B.H. Immunosuppression-induced leukoencephalopathy from tacrolimus (FK605). Ann Neurol 40 (1996) 575-580
54. Snyder S.H., Sabatini D.M., Lai M.M., Steiner J.P., Hamilton G.S., and Suzdak P.D. Neural actions of immunophilin ligands. Trends Pharmacol Sci 19 (1998) 21-26
55. Sterio D.C. The unbiased estimation of numbers and sizes of arbitrary particles using the disector. J Microsc 134 (1984) 127-136
56. Wenning G.K., Odin P., Morrish P., Rehncrona S., Widner H., Brundin P., Rothwell J.C., Brown R., Gustavii B., Hagell P., Jahanshahi M., Sale G., Björklund A., Brooks D.J., Marsden C.D., Quinn N.P., and Lindvall O. Short- and long-term survival and function of unilateral intrastriatal dopaminergic grafts in Parkinson's disease. Ann Neurol 42 (1997) 95-107
57. Widner H., Brundin P., Björklund A., and Moller E. Immunological aspects of neural grafting in the mammalian central nervous system. Prog Brain Res 78 (1988) 303-307
58. Willing A.E., Sudberry J.J., Othberg A.I., Saporta S., Poulos S.G., Cameron D.F., Freeman T.B., and Sanberg P.R. Sertoli cells decrease microglial response and increase engraftment of human hNT neurons in the hemiparkinsonian rat striatum. Brain Res Bull 48 (1999) 441-444
59. Winkler C., Kirik D., and Björklund A. Cell transplantation in Parkinson's disease: how can we make it work?. Trends Neurosci 28 (2005) 86-92
60. Winter C., Schenkel J., Burger E., Eickmeier C., Zimmermann M., and Herdegen T. The immunophilin ligand FK506, but not GPI-1046, protects against neuronal death and inhibits c-Jun expression in the substantia nigra pars compacta following transaction of the rat medial forebrain bundle. Neuroscience 95 (2000) 753-762
61. Wood M.J., Sloan D.J., Wood K.J., and Charlton H.M. Indefinite survival of neural xenografts induced with anti-CD4 monoclonal antibodies. Neuroscience 70 (1996) 775-789