Porcine fetal ventral mesencephalic cells are targets for primed xenoreactive human T cells

Cell Transplantation

Volumn 15, Issue 5, 2006, Pages 381-387

  Koopmans, Jan ^a   De Haan, Aalzen ^a   Bruin, Blinda ^a   Van Gun, Ieneke Der ^a   Van Dijk, Henk ^b   Rozing, Jan ^a   De Leij, Lou ^a   Staal, Michiel ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Antibody dependent cellular cytotoxicity (ADCC); Parkinson's disease; Porcine; T cells; Ventral mesencephalon; Xenotransplantation

Indexed keywords

CHROMIUM 51; DOPAMINE; INTERLEUKIN 2;

ALLOTRANSPLANTATION; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN PRESENTING CELL; ARTICLE; CELL SUSPENSION; CONTROLLED STUDY; CORPUS STRIATUM; CYTOLYSIS; FEMALE; FETUS; GRAFT SURVIVAL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREACTIVITY; INCUBATION TIME; MESENCEPHALON; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; NORMAL HUMAN; PARKINSON DISEASE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SPLEEN CELL; SWINE; XENOTRANSPLANTATION;

ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGEN-PRESENTING CELLS; CELLS, CULTURED; CYTOTOXICITY TESTS, IMMUNOLOGIC; FETAL TISSUE TRANSPLANTATION; HUMANS; INTERLEUKIN-2; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; MESENCEPHALON; SWINE; T-LYMPHOCYTES; TRANSPLANTATION, HETEROLOGOUS;

SUIDAE; SUS SCROFA;

EID: 33748284501     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000006783981846     Document Type: Article

References (52)

1. Bach, F. H.; Robson, S. C.; Winkler, H.; Ferran, C.; Stuhlmeier, K. M.; Wrighton, C. J.; Hancock, W. W. Barriers to xenotransplantation. Nat. Med. 1:869-873; 1995.
2. Bach, F. H.; Winkler, H.; Ferran, C.; Hancock, W. W.; Robson, S. C. Delayed xenograft rejection. Immunol. Today 17:379-384; 1996.
3. Barker, R. A.; Dunnett, S. B.; Faissner, A.; Fawcett, J. W. The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp. Neurol. 141:79-93; 1996.
4. Barker, R. A.; Dunnett, S. B.; Richards, A. The rejection of neural xenotransplants: A role for antibodies. Transplantation 68:1091-1092; 1999.
5. Barker, R. A.; Ratcliffe, E.; McLaughlin, M.; Richards, A.; Dunnett, S. B. A role for complement in the rejection of porcine ventral mesencephalic xenografts in a rat model of Parkinson's disease. J. Neurosci. 20:3415-3424; 2000.
6. Björklund, A.; Stenevi, U. Reconstruction of the nigrostriatal dopamine pathway by intracerebral nigral transplants. Brain Res. 177:555-560; 1979.
7. Brevig, T.; Kristensen, T.; Zimmer, J. Expression of major histocompatibility complex antigens and induction of human T-lymphocyte proliferation by astrocytes and macrophages from porcine fetal brain. Exp. Neurol. 159:474-483; 1999.
8. Brundin, P.; Widner, H.; Nilsson, O. G.; Strecker, R. E.; Björklund, A. Intracerebral xenografts of dopamine neurons: The role of immunosuppression and the blood-brain barrier. Exp. Brain Res. 75:195-207; 1989.
9. Cooke, S. P.; Pearson, J. D.; Savage, C. O. Human IgG xenoreactive antibodies mediate damage to porcine endothelial cells in vitro by both humoral and cellular mechanisms. Transpl. Immunol. 5:39-44; 1997.
10. Deacon, T.; Schumacher, J.; Dinsmore, J.; Thomas, C.; Palmer, P.; Kott, S.; Edge, A.; Penney, D.; Kassissieh, S.; Dempsey, P.; Isacson, O. Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nat. Med. 3:350-353; 1997.
11. DerSimonian, H.; Pan, L.; Yatko, C.; Rodrigue-Way, A.; Johnson, E.; Edge, A. S. Human anti-porcine T cell response: blocking with anti-class 1 antibody leads to hyporesponsiveness and a switch in cytokine production. J. Immunol. 162:6993-7001; 1999.
12. Duan, W. M.; Brundin, P.; Widner, H. Addition of allogeneic spleen cells causes rejection of intrastriatal embryonic mesencephalic allografts in the rat. Neuroscience 77:599-609; 1997.
13. Duan, W. M.; Widner, H.; Brundin, P. Temporal pattern of host responses against intrastriatal grafts of syngeneic, allogeneic or xenogeneic embryonic neuronal tissue in rats. Exp. Brain Res. 104:227-242; 1995.
14. Fink, J. S.; Schumacher, J. M.; Ellias, S. L.; Palmer, E. P.; Saint-Hilaire, M.; Shannon, K.; Penn, R.; Starr, P.; VanHorne, C.; Kott, H. S.; Dempsey, P. K.; Fischman, A. J.; Raineri, R.; Manhart, C.; Dinsmore, J.; Isacson, O. Porcine xenografts in Parkinson's disease and Huntington's disease patients: Preliminary results. Cell Transplant. 9:273-278; 2000.
15. Finsen, B. R. Microglial reactions following CNS-grafting. Clin. Neuropathol. 12:308-310; 1993.
16. Fischer, H. G.; Nitzgen, B.; Germann, T.; Degitz, K.; Daubener, W.; Hadding, U. Differentiation driven by granulocyte-macrophage colony-stimulating factor endows microglia with interferon-gamma-independent antigen presentation function. J. Neuroimmunol. 42:87-95; 1993.
17. Freeman, T. B.; Olanow, C. W.; Hauser, R. A.; Nauert, G. M.; Smith, D. A.; Borlongan, C. V.; Sanberg, P. R.; Holt, D. A.; Kordower, J. H.; Vingerhoets, F. J. Bilateral fetal nigral transplantation into the postcommissural putamen in Parkinson's disease. Ann. Neurol. 38:379-388; 1995.
18. Galpern, W. R.; Burns, L. H.; Deacon, T. W.; Dinsmore, J.; Isacson, O. Xenotransplantation of porcine fetal ventral mesencephalon in a rat model of Parkinson's disease: Functional recovery and graft morphology. Exp. Neurol. 140:1-13; 1996.
19. HogenEsch, R. I.; Koopmans, J.; Copray, J. C.; van Roon, W. M.; Kema, I.; Molenaar, G.; Go, K. G.; Staal, M. J. Fetal porcine ventral mesencephalon graft. Determination of the optimal gestational age for implantation in parkinsonian patients. Exp. Brain Res. 132:345-350; 2000.
20. HogenEsch, R. I.; Staal, M. J.; Kema, I. P.; Buys, C. H.; Go, K. G. Utility of fragmented human fetal tissue as a potential dopaminergic brain graft in Parkinson's disease. Stereotact. Funct. Neurosurg. 61:1-11; 1993.
21. Huffaker, T. K.; Boss, B. D.; Morgan, A. S.; Neff, N. T.; Strecker, R. E.; Spence, M. S.; Miao, R. Xenografting of fetal pig ventral mesencephalon corrects motor asymmetry in the rat model of Parkinson's disease. Exp. Brain Res. 77:329-336; 1989.
22. Kawamoto, J. C.; Barrett, J. N. Cryopreservation of primary neurons for tissue culture. Brain Res. 384:84-93; 1986.
23. Kirk, A. D.; Li, R. A.; Kinch, M. S.; Abernethy, K. A.; Doyle, C.; Bollinger, R. R. The human antiporcine cellular repertoire. In vitro studies of acquired and innate cellular responsiveness. Transplantation 55:924-931; 1993.
24. Koopmans, J.; de Haan, A.; Bruin, E.; van der Gun, I.; van Dijk, H.; Rozing, J.; de Leij, L.; Staal, M. Individual human serum differs in the amount of antibodies with affinity for pig fetal ventral mesencephalic cells and the ability to lyse these cells by complement activation. Cell Transplant. 13:631-637; 2004.
25. Koopmans, J.; HogenEsch, I.; Copray, S.; Middel, B.; van Dijk, H.; Go, K. G.; Staal, M. Cryopreservation of porcine fetal ventral mesencephalic tissue for intrastriatal transplantation in Parkinson's disease. Cell Transplant. 10:573-581; 2001.
26. Kordower, J. H.; Freeman, T. B.; Chen, E. Y.; Mufson, E. J.; Sanberg, P. R.; Hauser, R. A.; Snow, B.; Olanow, C. W. Fetal nigral grafts survive and mediate clinical benefit in a patient with Parkinson's disease. Mov. Disord. 13:383-393; 1998.
27. Kumagai, B. M.; Satake, M.; Qian, Y.; Holgersson, J.; Moller, E. Human NK cell and ADCC reactivity against xenogeneic porcine target cells including fetal porcine islet cells. Xenotransplantation 5:132-145; 1998.
28. Larsson, L. C.; Czech, K. A.; Widner, H.; Korsgren, O. Discordant neural tissue xenografts survive longer in immunoglobulin deficient mice. Transplantation 68:1153-1160; 1999.
29. Larsson, L. C.; Duan, W. M.; Widner, H. Discordant xenografts: Different outcome after mouse and rat neural tissue transplantation to guinea-pigs. Brain Res. Bull. 49:367-376; 1999.
30. Mahalik, T. J.; Hahn, W. E.; Clayton, G. H.; Owens, G. P. Programmed cell death in developing grafts of fetal substantia nigra. Exp. Neurol. 129:27-36; 1994.
31. Molenaar, G. J.; HogenEsch, R. I.; Sprengers, M. E.; Staal, M. J. Ontogenesis of embryonic porcine ventral mesencephalon in the perspective of its potential use as a xenograft in Parkinson's disease. J. Comp. Neurol. 382:19-28; 1997.
32. Ni, H. T.; Merica, R. R.; Spellman, S. R.; Wang, J. M.; Low, W. C. Visualization of antigen-specific T cell activation in vivo in response to intracerebral administration of a xenopeptide. Exp. Neurol. 164:362-370; 2000.
33. Ostergaard, K.; Holm, I. E.; Zimmer, J. Tyrosine hydroxylase and acetylcholinesterase in the domestic pig mesencephalon: An immunocytochemical and histochemical study. J. Comp. Neurol. 322:149-166; 1992.
34. Pakzaban, P.; Deacon, T. W.; Burns, L. H.; Dinsmore, J.; 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 65:983-996; 1995.
35. Perlow, M. J.; Freed, W. J.; Hoffer, B. J.; Seiger, A.; Olson, L.; Wyatt, R. J. Brain grafts reduce motor abnormalities produced by destruction of nigrostriatal dopamine system. Science 204:643-647; 1979.
36. Peschanski, M.; Defer, G.; N'Guyen, J. P.; Ricolfi, F.; Monfort, J. C.; Remy, P.; Geny, C.; Samson, Y.; Hantraye, P.; Jeny, R. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson's disease following intrastriatal transplantation of foetal ventral mesencephalon. Brain 117:487-499; 1994.
37. Platt, J. L.; Fischel, R. J.; Matas, A. J.; Reif, S. A.; Bolman, R. M.; Bach, F. H. Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation 52:214-220; 1991.
38. Platt, J. L.; Lin, S. S.; McGregor, C. G. Acute vascular rejection. Xenotransplantation 5:169-175; 1998.
39. Remy, S.; Canova, C.; Daguin-Nerriere, V.; Martin, C.; Melchior, B.; Neveu, I.; Charreau, B.; Soulillou, J. P.; Brachet, P. Different mechanisms mediate the rejection of porcine neurons and endothelial cells transplanted into the rat brain. Xenotransplantation 8:136-148; 2001.
40. Samali, A.; Gorman, A. M.; Cotter, T. G. Apoptosis-the story so far... Experientia 52:933-941; 1996.
41. Sauer, H.; Frodl, E. M.; Kupsch, A.; ten Bruggencate, G.; Oertel, W. H. Cryopreservation, survival and function of intrastriatal fetal mesencephalic grafts in a rat model of Parkinson's disease. Exp. Brain Res. 90:54-62; 1992.
42. 18F]6-L-fluorodopa studies in two patients with putaminal implants. Ann. Neurol. 31:166-173; 1992.
43. Schaapherder, A. F.; Daha, M. R.; te Bulte, M. T.; vander-Woude, F. J.; Gooszen, H. G. Antibody-dependent cell-mediated cytotoxicity against porcine endothelium induced by a majority of human sera. Transplantation 57:1376-1382; $.
44. 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.; Isacson, O. Transplantation of embryonic porcine mesencephalic tissue in patients with PD. Neurology 54:1042-1050; 2000.
45. Shrestha, A.; Horino, K.; Nishiura, H.; Yamamoto, T. Acquired immune response as a consequence of the macrophage-dependent apoptotic cell clearance and role of the monocyte chemotactic S19 ribosomal protein dimer in this connection. Lab. Invest. 79:1629-1642; 1999.
46. Sortwell, C. E.; Pitzer, M. R.; Collier, T. J. Time course of apoptotic cell death within mesencephalic cell suspension grafts: Implications for improving grafted dopamine neuron survival. Exp. Neurol. 165:268-277; 2000.
47. Sumitran, S.; Anderson, P.; Widner, H.; Holgersson, J. Porcine embryonic brain cell cytotoxicity mediated by human natural killer cells. Cell Transplant. 8:601-610; 1999.
48. Sumitran, S.; Liu, J.; Czech, K. A.; Christensson, B.; Widner, H.; Holgersson, J. Human natural antibodies cytotoxic to pig embryonic brain cells recognize novel non-Galalpha1,3Gal-based xenoantigens. Exp. Neurol. 159:347-361; 1999.
49. van Roon, W. M. C.; Copray, J. C. V. M.; HogenEsch, R. I.; Staal, M. J.; Go, K. G. Fetal porcine mesencephalon grafts: Dissection procedure and cellular characterization in culture. Restor. Neurol. Neurosci. 7:199-205; 1995.
50. Widner, H.; Tetrud, J.; Rehncrona, S.; Snow, B.; Brundin, P.; Gustavii, B.; Björklund, A.; Lindvall, O.; Langsten, J. W. Bilateral fetal mesencephalic grafting in two patients with parkinsonism induced by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). N. Engl. J. Med. 327:1556-1563; 1992.
51. Yi, S.; Feng, X.; Wang, Y.; Kay, T. W.; O'Connell, P. J. CD4+ cells play a major role in xenogeneic human anti-pig cytotoxicity through the Fas/Fas ligand lytic pathway. Transplantation 67:435-443; 1999.
52. Zawada, W. M.; Zastrow, D. J.; Clarkson, E. D.; Adams, F. S.; Bell, K. P.; Freed, C. R. Growth factors improve immediate survival of embryonic dopamine neurons after transplantation into rats. Brain Res. 786:96-103; 1998.