Critical role of natural killer cells in the rejection of human hepatocytes after xenotransplantation into immunodeficient mice

Transplant International

Volumn 23, Issue 9, 2010, Pages 934-943

  Kawahara, Toshiyasu ^a   Douglas, Donna N ^a   Lewis, Jamie ^a   Lund, Garry ^b   Addison, William ^c   Tyrrell, David Lorne ^b,c   Churchill, Thomas A ^a,c   Kneteman, Norman M ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b KMT Hepatech Inc   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

cell transplantation; hepatocyte transplantation; humanized mice; natural killer cell; xenotransplantation

Indexed keywords

ALPHA 1 ANTICHYMOTRYPSIN; IODINE 125; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PLASMINOGEN ACTIVATOR; UROKINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL TRANSPLANTATION; CONTROLLED STUDY; GRAFT FAILURE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; LIVER CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SCID MOUSE; XENOTRANSPLANTATION;

ANIMALS; DISEASE MODELS, ANIMAL; HEPATOCYTES; HUMANS; IMMUNOHISTOCHEMISTRY; KILLER CELLS, NATURAL; LIVER TRANSPLANTATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; PHENOTYPE; SEVERE COMBINED IMMUNODEFICIENCY; TRANSPLANTATION, HETEROLOGOUS;

EID: 77955262883     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/j.1432-2277.2010.01063.x     Document Type: Article

References (50)

1. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007 7 : 118.
2. Heckel JL, Sandgren EP, Degen JL, Palmiter RD, Brinster RL. Neonatal bleeding in transgenic mice expressing urokinase-type plasminogen activator. Cell 1990 62 : 447.
3. Sandgren EP, Palmiter RD, Heckel JL, Daugherty CC, Brinster RL, Degen JL. Complete hepatic regeneration after somatic deletion of an albumin-plasminogen activator transgene. Cell 1991 66 : 245.
4. Rhim JA, Sandgren EP, Palmiter RD, Brinster RL. Complete reconstitution of mouse liver with xenogeneic hepatocytes. Proc Natl Acad Sci USA 1995 92 : 4942.
5. Dandri M, Burda MR, Torok E, et al. Repopulation of mouse liver with human hepatocytes and in vivo infection with hepatitis B virus. Hepatology 2001 33 : 981.
6. Mercer DF, Schiller DE, Elliott JF, et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001 7 : 927.
7. Kneteman NM, Weiner AJ, O'Connell J, et al. Anti-HCV therapies in chimeric scid-Alb/uPA mice parallel outcomes in human clinical application. Hepatology 2006 43 : 1346.
8. Sacci JJB, Alam U, Douglas D, et al. Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. Int J Parasitol 2006 36 : 353.
9. Morosan S, Hez-Deroubaix S, Lunel F, et al. Liver-stage development of Plasmodium falciparum, in a humanized mouse model. J Infect Dis 2006 193 : 996.
10. Hsu EC, Hsi B, Hirota-Tsuchihara M, et al. Modified apoptotic molecule (BID) reduces hepatitis C virus infection in mice with chimeric human livers. Nat Biotechnol 2003 21 : 519.
11. Law M, Maruyama T, Lewis J, et al. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 2008 14 : 25.
12. Inoue K, Umehara T, Ruegg UT, et al. Evaluation of a cyclophilin inhibitor in hepatitis C virus-infected chimeric mice in vivo. Hepatology 2007 45 : 921.
13. Tateno C, Yoshizane Y, Saito N, et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am J Pathol 2004 165 : 901.
14. Orange JS, Fassett MS, Koopman LA, Boyson JE, Strominger JL. Viral evasion of natural killer cells. Nat Immunol 2002 3 : 1006.
15. Smyth MJ, Hayakawa Y, Takeda K, Yagita H. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2002 2 : 850.
16. Hamerman JA, Ogasawara K, Lanier LL. NK cells in innate immunity. Curr Opin Immunol 2005 17 : 29.
17. Kirk A, Heinle J, Mault J, Sanfilippo F. Ex vivo characterization of human anti-porcine hyperacute cardiac rejection. Transplantation 1993 56 : 785.
18. Khalfoun B, Barrat D, Watier H, et al. Development of an ex vivo model of pig kidney perfused with human lymphocytes. Analysis of xenogeneic cellular reactions. Surgery 2000 128 : 447.
19. Itescu S, Kwiatkowski P, Artrip JH, et al. Role of natural killer cells, macrophages, and accessory molecule interactions in the rejection of pig-to-primate xenografts beyond the hyperacute period. Hum Immunol 1998 59 : 275.
20. Gourlay WA, Chambers WH, Monaco AP, Maki T. Importance of natural killer cells in the rejection of hamster skin xenografts. Transplantation 1998 65 : 727.
21. Candinas D, Belliveau S, Koyamada N, et al. T cell independence of macrophage and natural killer cell infiltration, cytokine production, and endothelial activation during delayed xenograft rejection. Transplantation 1996 62 : 1920.
22. Kuwaki K, Tseng Y-L, Dor FJMF, et al. Heart transplantation in baboons using α1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat Med 2005 11 : 29.
23. Yamada K, Yazawa K, Shimizu A, et al. Marked prolongation of porcine renal xenograft survival in baboons through the use ofα1,3- galactosyltransferase gene-knockout donors and the cotransplantation of vascularized thymic tissue. Nat Med 2005 11 : 32.
24. Schroeder C, Allan J, Nguyen B, et al. Hyperacute rejection is attenuated in GalT knockout swine lungs perfused ex vivo with human blood. Transplant Proc 2005 37 : 512.
25. Baumann BC, Forte P, Hawley RJ, Rieben R, Schneider MKJ, Seebach JD. Lack of galactose-α-1,3-galactose expression on porcine endothelial cells prevents complement-induced lysis but not direct xenogeneic NK cytotoxicity. J Immunol 2004 172 : 6460.
26. Zhong H, Cecilia E, Makiko K-B, Khalid BI, Jan H. Aberrant expression of alpha-Gal on primary human endothelium does not confer susceptibility to NK cell cytotoxicity or increased NK cell adhesion. Eur J Immunol 2004 34 : 1185.
27. Cao X, Shores EW, Hu-Li J, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor γ chain. Immunity 1995 2 : 223.
28. Meuleman P, Vanlandschoot P, Leroux-Roels G. A simple and rapid method to determine the zygosity of uPA-transgenic SCID mice. Biochem Biophys Res Commun 2003 308 : 375.
29. Kawahara T, Rodriguez-Barbosa JI, Zhao Y, Zhao G, Sykes M. Global unresponsiveness as a mechanism of natural killer cell tolerance in mixed xenogeneic chimeras. Am J Transplant 2007 7 : 2090.
30. Shao C, Deng L, Henegariu O, et al. Mitotic recombination produces the majority of recessive fibroblast variants in heterozygous mice. Proc Natl Acad Sci USA 1999 96 : 9230.
31. Perou CM, Justice MJ, Pryor RJ, Kaplan J. Complementation of the beige mutation in cultured cells by episomally replicating murine yeast artificial chromosomes. Proc Natl Acad Sci USA 1996 93 : 5905.
32. Fisher RA, Stephen CS. Human hepatocyte transplantation: worldwide results. Transplantation 2006 82 : 441.
33. Kneteman NM, Mercer DF. Mice with chimeric human livers: who says supermodels have to be tall? Hepatology 2005 41 : 703.
34. Bissig K-D, Le TT, Woods N-B, Verma IM. Repopulation of adult and neonatal mice with human hepatocytes: a chimeric animal model. Proc Natl Acad Sci USA 2007 104 : 20507.
35. Cascalho M, Platt JL. The immunological barrier to xenotransplantation. Immunity 2001 14 : 437.
36. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002 3 : 1150.
37. Dawson J, Vidal A, Malyguine A. Natural killer cell-endothelial cell interactions in xenotransplantation. Immunol Res 2000 22 : 165.
38. -/- double-mutant mice. Blood 2003 102 : 2522.
39. Talmadge JE, Meyers KM, Prieur DJ, Starkey JR. Role of NK cells in tumour growth and metastasis in beige mice. Nature 1980 284 : 622.
40. Barbosa MDFS, Nguyen QA, Tchernev VT, et al. Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 1996 382 : 262.
41. Scharton-Kersten TM, Sher A. Role of natural killer cells in innate resistance to protozoan infections. Curr Opin Immunol 1997 9 : 44.
42. Bannai M, Oya H, Kawamura T, et al. Disparate effect of beige mutation on cytotoxic function between natural killer and natural killer T cells. Immunology 2000 100 : 165.
43. Ming-Lee L, Yifan Z, Stephen LN, et al. NK cells promote peritoneal xenograft rejection through an IFN-γ-dependent mechanism. Xenotransplantation 2006 13 : 536.
44. Caiazzo R, Gmyr V, Kremer B, et al. Quantitative in vivo islet potency assay in normoglycemic nude mice correlates with primary graft function after clinical transplantation. Transplantation 2008 86 : 360.
45. Cheers C, Wood P. Listeriosis in beige mice and their heterozygous littermates. Immunology 1984 51 : 711.
46. Turner WJD, Chatten J, Lampson LA. Human neuroblastoma cell growth in xenogeneic hosts: comparison of T cell-deficient and NK-deficient hosts, and subcutaneous or intravenous injection routes. J Neurooncol 1990 8 : 121.
47. Seebach JD, Comrack C, Germana S, LeGuern C, Sachs DH, DerSimonian H. HLA-Cw3 expression on porcine endothelial cells protects against xenogeneic cytotoxicity mediated by a subset of human NK cells. J Immunol 1997 159 : 3655.
48. Anthony D, Nicola JM, Robert IL. HLA-G inhibits the transendothelial migration of human NK cells. Eur J Immunol 2000 30 : 586.
49. Pietro F, Bettina CB, Elisabeth HW, Seebach JD. HLA-E expression on porcine cells: protection from human NK cytotoxicity depends on peptide loading. Am J Transplant 2005 5 : 2085.
50. Forte P, Lilienfeld BG, Baumann BC, Seebach JD. Human NK cytotoxicity against porcine cells is triggered by NKp44 and NKG2D. J Immunol 2005 175 : 5463.