Neonatal immune-tolerance in mice does not prevent xenograft rejection

Experimental Neurology

Volumn 254, Issue , 2014, Pages 90-98

  Mattis, Virginia B ^a   Wakeman, Dustin R ^b   Tom, Colton ^a   Dodiya, Hemraj B ^b   Yeung, Sylvia Y ^c   Tran, Andrew H ^c   Bernau, Ksenija ^d   Ornelas, Loren ^a   Sahabian, Anais ^a   Reidling, Jack ^c   Sareen, Dhruv ^a   Thompson, Leslie M ^c   Kordower, Jeffrey H ^b   Svendsen, Clive N ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b RUSH UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Huntington's disease; Immune rejection; Neonatal immunity; Neonatal tolerance; Xenograft

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; GRAFT REJECTION; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; MOUSE; MOUSE STRAIN; NEURAL STEM CELL; NEWBORN; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; TRANSGENIC MOUSE; XENOGRAFT;

HUNTINGTON'S DISEASE; IMMUNE REJECTION; NEONATAL IMMUNITY; NEONATAL TOLERANCE; XENOGRAFT;

ANIMALS; ANIMALS, NEWBORN; ANIMALS, OUTBRED STRAINS; CELLS, CULTURED; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; FEMALE; GRAFT REJECTION; GRAFT SURVIVAL; HETEROGRAFTS; HUMANS; HUNTINGTON DISEASE; IMMUNE TOLERANCE; MALE; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NUCLEAR PROTEINS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84893609567     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.01.007     Document Type: Article

References (46)

1. Behrstock S., Ebert A.D., Klein S., Schmitt M., Moore J.M., Svendsen C.N. Lesion-induced increase in survival and migration of human neural progenitor cells releasing GDNF. Cell Transplant. 2008, 17:753-762.
2. Capowski E.E., Schneider B.L., Ebert A.D., Seehus C.R., Szulc J., Zufferey R., Aebischer P., Svendsen C.N. Lentiviral vector-mediated genetic modification of human neural progenitor cells for ex vivo gene therapy. J. Neurosci. Methods 2007, 163:338-349.
3. Carletti B., Grimaldi P., Magrassi L., Rossi F. Engraftment and differentiation of neocortical progenitor cells transplanted to the embryonic brain in utero. J. Neurocytol. 2004, 33:309-319.
4. Denham M., Parish C.L., Leaw B., Wright J., Reid C.A., Petrou S., Dottori M., Thompson L.H. Neurons derived from human embryonic stem cells extend long-distance axonal projections through growth along host white matter tracts after intra-cerebral transplantation. Front. Cell. Neurosci. 2012, 6:11.
5. Ebert A.D., Yu J., Rose F.F., Mattis V.B., Lorson C.L., Thomson J.A., Svendsen C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457:277-280.
6. Emborg M.E., Liu Y., Xi J., Zhang X., Yin Y., Lu J., Joers V., Swanson C., Holden J.E., Zhang S.C. Induced pluripotent stem cell-derived neural cells survive and mature in the nonhuman primate brain. Cell Rep. 2013, 3:646-650.
7. Englund U., Fricker-Gates R.A., Lundberg C., Bjorklund A., Wictorin K. Transplantation of human neural progenitor cells into the neonatal rat brain: extensive migration and differentiation with long-distance axonal projections. Exp. Neurol. 2002, 173:1-21.
8. French A.E., Soldin S.J., Soldin O.P., Koren G. Milk transfer and neonatal safety of tacrolimus. Ann. Pharmacother. 2003, 37:815-818.
9. Jablonska A., Kozlowska H., Markiewicz I., Domanska-Janik K., Lukomska B. Transplantation of neural stem cells derived from human cord blood to the brain of adult and neonatal rats. Acta Neurobiol. Exp. (Wars) 2010, 70:337-350.
10. Janowski M., Jablonska A., Kozlowska H., Orukari I., Bernard S., Bulte J.W., Lukomska B., Walczak P. Neonatal desensitization does not universally prevent xenograft rejection. Nat. Methods 2012, 9:856-858. author reply 858.
11. Kallur T., Darsalia V., Lindvall O., Kokaia Z. Human fetal cortical and striatal neural stem cells generate region-specific neurons in vitro and differentiate extensively to neurons after intrastriatal transplantation in neonatal rats. J. Neurosci. Res. 2006, 84:1630-1644.
12. Kelly C.M., Precious S.V., Scherf C., Penketh R., Amso N.N., Battersby A., Allen N.D., Dunnett S.B., Rosser A.E. Neonatal desensitization allows long-term survival of neural xenotransplants without immunosuppression. Nat. Methods 2009, 6:271-273.
13. Klein S.M., Behrstock S., McHugh J., Hoffmann K., Wallace K., Suzuki M., Aebischer P., Svendsen C.N. GDNF delivery using human neural progenitor cells in a rat model of ALS. Hum. Gene Ther. 2005, 16:509-521.
14. Kopen G.C., Prockop D.J., Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:10711-10716.
15. Kriks S., Shim J.W., Piao J., Ganat Y.M., Wakeman D.R., Xie Z., Carrillo-Reid L., Auyeung G., Antonacci C., Buch A., Yang L., Beal M.F., Surmeier D.J., Kordower J.H., Tabar V., Studer L. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011, 480:547-551.
16. Liew C.G., Draper J.S., Walsh J., Moore H., Andrews P.W. Transient and stable transgene expression in human embryonic stem cells. Stem Cells 2007, 25:1521-1528.
17. Lundberg C., Englund U., Trono D., Bjorklund A., Wictorin K. Differentiation of the RN33B cell line into forebrain projection neurons after transplantation into the neonatal rat brain. Exp. Neurol. 2002, 175:370-387.
18. Marcus A.J., Coyne T.M., Black I.B., Woodbury D. Fate of amnion-derived stem cells transplanted to the fetal rat brain: migration, survival and differentiation. J. Cell. Mol. Med. 2008, 12:1256-1264.
19. Mattis V.B., Svendsen C.N. Induced pluripotent stem cells: a new revolution for clinical neurology?. Lancet Neurol. 2011, 10:383-394.
20. McBride J.L., Behrstock S.P., Chen E.Y., Jakel R.J., Siegel I., Svendsen C.N., Kordower J.H. Human neural stem cell transplants improve motor function in a rat model of Huntington's disease. J. Comp. Neurol. 2004, 475:211-219.
21. Muotri A.R., Nakashima K., Toni N., Sandler V.M., Gage F.H. Development of functional human embryonic stem cell-derived neurons in mouse brain. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18644-18648.
22. Nijagal A., Wegorzewska M., Le T., Tang Q., Mackenzie T.C. The maternal immune response inhibits the success of in utero hematopoietic cell transplantation. Chimerism 2011, 2:55-57.
23. Ostenfeld T., Caldwell M.A., Prowse K.R., Linskens M.H., Jauniaux E., Svendsen C.N. Human neural precursor cells express low levels of telomerase in vitro and show diminishing cell proliferation with extensive axonal outgrowth following transplantation. Exp. Neurol. 2000, 164:215-226.
24. Passini M.A., Wolfe J.H. Widespread gene delivery and structure-specific patterns of expression in the brain after intraventricular injections of neonatal mice with an adeno-associated virus vector. J. Virol. 2001, 75:12382-12392.
25. Peiguo Z., Shijie Z., Liang M. Chimerism but not neonatal antigen exposure induces transplant tolerance. Scand. J. Immunol. 2012, 76:108-112.
26. Rachubinski A.L., Maclean K.N., Evans J.R., Bjugstad K.B. Modulating cognitive deficits and tau accumulation in a mouse model of aging Down syndrome through neonatal implantation of neural progenitor cells. Exp. Gerontol. 2012, 47:723-733.
27. Ramaswamy S., McBride J.L., Han I., Berry-Kravis E.M., Zhou L., Herzog C.D., Gasmi M., Bartus R.T., Kordower J.H. Intrastriatal CERE-120 (AAV-Neurturin) protects striatal and cortical neurons and delays motor deficits in a transgenic mouse model of Huntington's disease. Neurobiol. Dis. 2009, 34:40-50.
28. Ridge J.P., Fuchs E.J., Matzinger P. Neonatal Tolerance Revisited: Turning on Newborn T Cells with Dendritic Cells. Science 1996, 271:1723-1726.
29. Roberton V.H., Evans A.E., Harrison D.J., Precious S.V., Dunnett S.B., Kelly C.M., Rosser A.E. Is the adult mouse striatum a hostile host for neural transplant survival?. Neuroreport 2013, 24:1010-1015.
30. Rosenstock T.R., de Brito O.M., Lombardi V., Louros S., Ribeiro M., Almeida S., Ferreira I.L., Oliveira C.R., Rego A.C. FK506 ameliorates cell death features in Huntington's disease striatal cell models. Neurochem. Int. 2011, 59:600-609.
31. Sim F.J., McClain C.R., Schanz S.J., Protack T.L., Windrem M.S., Goldman S.A. CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat. Biotechnol. 2011, 29:934-941.
32. Streilein J.W. Neonatal tolerance: towards an immunogenetic definition of self. Immunol. Rev. 1979, 46:123-146.
33. Sundberg M., Bogetofte H., Lawson T., Jansson J., Smith G., Astradsson A., Moore M., Osborn T., Cooper O., Spealman R., Hallett P., Isacson O. Improved cell therapy protocol for Parkinson's disease based on differentiation efficiency and safety of Hesc-, Hipsc and non-human primate Ipsc-derived DA neurons. Stem Cells 2013, 31:1548-1562.
34. Suzuki M., McHugh J., Tork C., Shelley B., Klein S.M., Aebischer P., Svendsen C.N. GDNF secreting human neural progenitor cells protect dying motor neurons, but not their projection to muscle, in a rat model of familial ALS. PLoS ONE 2007, 2:e689.
35. Svendsen C.N. Back to the future: how human induced pluripotent stem cells will transform regenerative medicine. Hum. Mol. Genet. 2013, 22(R1):R32-R38.
36. Svendsen C.N., Caldwell M.A., Shen J., ter Borg M.G., Rosser A.E., Tyers P., Karmiol S., Dunnett S.B. Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson's disease. Exp. Neurol. 1997, 148:135-146.
37. Svendsen C.N., ter Borg M.G., Armstrong R.J., Rosser A.E., Chandran S., Ostenfeld T., Caldwell M.A. A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 1998, 85:141-152.
38. Tamaki S., Eckert K., He D., Sutton R., Doshe M., Jain G., Tushinski R., Reitsma M., Harris B., Tsukamoto A., Gage F., Weissman I., Uchida N. Engraftment of sorted/expanded human central nervous system stem cells from fetal brain. J. Neurosci. Res. 2002, 69:976-986.
39. The_HD_iPSC_Consortium Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 2012, 11:264-278.
40. Tregoning John S. Neonatal Immunity. In: Encyclopedia of Life Sciences (ELS) December 2009, Chichester, John Wiley & Sons, Ltd.
41. Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., Weissman I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14720-14725.
42. Wakeman D.R., Hofmann M.R., Redmond D.E., Teng Y.D., Snyder E.Y. Long-term multilayer adherent network (MAN) expansion, maintenance, and characterization, chemical and genetic manipulation, and transplantation of human fetal forebrain neural stem cells. Curr. Protoc. Stem Cell Biol. 2009, 9. D.3.1-2D.3.77.
43. Wang S., Bates J., Li X., Schanz S., Chandler-Militello D., Levine C., Maherali N., Studer L., Hochedlinger K., Windrem M., Goldman S.A. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013, 12:252-264.
44. Windrem M.S., Nunes M.C., Rashbaum W.K., Schwartz T.H., Goodman R.A., McKhann G., Roy N.S., Goldman S.A. Fetal and adult human oligodendrocyte progenitor cell isolates myelinate the congenitally dysmyelinated brain. Nat. Med. 2004, 10:93-97.
45. Windrem M.S., Schanz S.J., Guo M., Tian G.F., Washco V., Stanwood N., Rasband M., Roy N.S., Nedergaard M., Havton L.A., Wang S., Goldman S.A. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell 2008, 2:553-565.
46. Zhang S., Jiang Y.Z., Zhang W., Chen L., Tong T., Liu W., Mu Q., Liu H., Ji J., Ouyang H.W., Zou X. Neonatal desensitization supports long-term survival and functional integration of human embryonic stem cell-derived mesenchymal stem cells in rat joint cartilage without immunosuppression. Stem Cells Dev. 2013, 22:90-101.