Clinical-scale isolation of interleukin-2-stimulated liver natural killer cells for treatment of liver transplantation with hepatocellular carcinoma

Cell Transplantation

Volumn 21, Issue 7, 2012, Pages 1397-1406

  Ohira, Masahiro ^a   Nishida, Seigo ^a   Tryphonopoulos, Panagiotis ^a   Tekin, Akin ^a   Selvaggi, Gennaro ^a   Moon, Jang ^a   Levi, David ^a   Ricordi, Camillo ^a   Ishiyama, Kohei ^b   Tanaka, Yuka ^b   Ohdan, Hideki ^b   Tzakis, Andreas G ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Current good manufacturing practice (cGMP); Hepatocellular carcinoma; Immunotherapy; Innate immunity; Natural killer cell

Indexed keywords

CD16 ANTIGEN; CD69 ANTIGEN; CD94 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; OKT 3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADOPTIVE IMMUNOTHERAPY; ADULT; AGED; ARTICLE; CANCER RECURRENCE; CELL POPULATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; GOOD MANUFACTURING PRACTICE; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; LIVER CELL CARCINOMA; LIVER PERFUSION; LIVER TRANSPLANTATION; MALE; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ADULT; AGED; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CYTOKINES; FEMALE; GRAFT REJECTION; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-2; K562 CELLS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LEUKOCYTES, MONONUCLEAR; LIVER; LIVER NEOPLASMS; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; RECURRENCE; TISSUE DONORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION; YOUNG ADULT;

EID: 84868549488     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X627589     Document Type: Article

References (48)

1. Balch, C. M.; Tilden, A. B.; Dougherty, P. A.; Cloud, G. A.; Abo, T. Heterogeneity of natural killer lymphocyte abnormalities in colon cancer patients. Surgery 95(1):63-70; 1984.
2. Bosma, B. M.; Metselaar, H. J.; Mancham, S.; Boor, P. P.; Kusters, J. G.; Kazemier, G.; Tilanus, H. W.; Kuipers, E. J.; Kwekkeboom, J. Characterization of human liver dendritic cells in liver grafts and perfusates. Liver Transpl. 12(3):384-393; 2006.
3. Bryceson, Y. T.; March, M. E.; Ljunggren, H. G.; Long, E. O. Synergy among receptors on resting natural killer (NK) cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107(1):159-166; 2006.
4. Buchwald, P.; Wang, X.; Khan, A.; Bernal, A.; Fraker, C.; Inverardi, L.; Ricordi, C. Quantitative assessment of islet cell products: Estimating the accuracy of the existing protocol and accounting for islet size distribution. Cell Transplant. 18(10):1223-1235; 2009.
5. Cai, L.; Zhang, Z.; Zhou, L.; Wang, H.; Fu, J.; Zhang, S.; Shi, M.; Zhang, H.; Yang, Y.; Wu, H.; Tien, P.; Wang, S. Functional impairment in circulating and intrahepatic natural killer (NK) cells and relative mechanism in hepatocellular carcinoma patients. Clin. Immunol. 129(3):428-437; 2008.
6. Chang, T. W.; Kung, P. C.; Gingras, S. P.; Goldstein, G. Does OKT3 monoclonal antibody react with an antigen-recognition structure on human T cells? Proc. Natl. Acad. Sci. USA 78(3):1805-1808; 1981.
7. Chatenoud, L.; Ferran, C.; Legendre, C.; Thouard, I.; Merite, S.; Reuter, A.; Gevaert, Y.; Kreis, H.; Franchimont, P.; Bach, J. F. In vivo cell activation following OKT3 administration. Systemic cytokine release and modulation by corticosteroids. Transplantation 49(4):697-702; 1990.
8. Collins, Jr., R. H.; Goldstein, S.; Giralt, S.; Levine, J.; Porter, D.; Drobyski, W.; Barrett, J.; Johnson, M.; Kirk, A.; Horowitz, M.; Parker, P. Donor leukocyte infusions in acute lymphocytic leukemia. Bone Marrow Transplant. 26(5):511-516; 2000.
9. Estrada, E. J.; Valacchi, F.; Nicora, E.; Brieva, S.; Esteve, C.; Echevarria, L.; Froud, T.; Bernetti, K.; Cayetano, S. M.; Velazquez, O.; Alejandro, R.; Ricordi, C. Combined treatment of intrapancreatic autologous bone marrow stem cells and hyperbaric oxygen in type 2 diabetes mellitus. Cell Transplant. 17(12):1295-1304; 2008.
10. Farag, S. S.; Caligiuri, M. A. Human natural killer cell development and biology. Blood Rev. 20(3):123-137; 2006.
11. Frohn, C.; Doehn, C.; Durek, C.; Bohle, A.; Schlenke, P.; Jocham, D.; Kirchner, H. Feasibility of the adoptive transfusion of allogenic human leukocyte antigen-matched natural killer cells in patients with renal cell carcinoma. J. Immunother. 23(4):499-504; 2000.
12. Harada, N.; Shimada, M.; Okano, S.; Suehiro, T.; Soejima, Y.; Tomita, Y.; Maehara, Y. Interleukin (IL)-12 gene therapy is an effective therapeutic strategy for hepatocellular carcinoma in immunosuppressed mice. J. Immunol. 173(11):6635-6644; 2004.
13. Hirata, M.; Kita, Y.; Saito, S.; Nishimura, M.; Ito, M.; Mizuta, K.; Tanaka, H.; Harihara, Y.; Kawarasaki, H.; Hashizume, K.; Makuuchi, M. Increase in natural killer cell activity following living-related liver transplantation. Transpl. Int. 11(Suppl. 1):S185-188; 1998.
14. Horn, M.; Phebus, C.; Blatt, J. Cancer chemotherapy after solid organ transplantation. Cancer 66(7):1468-1471; 1990.
15. Horowitz, M. M.; Gale, R. P.; Sondel, P. M.; Goldman, J. M.; Kersey, J.; Kolb, H. J.; Rimm, A. A.; Ringden, O.; Rozman, C.; Speck, B.; Truitt, R.; Zwaan, F.; Bortin, M. Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75(3):555-562; 1990.
16. Ioannou, G. N.; Perkins, J. D.; Carithers, Jr., R. L. Liver transplantation for hepatocellular carcinoma: Impact of the model for End-Stage Liver Disease (MELD) allocation system and predictors of survival. Gastroenterology 134(5):1342-1351; 2008.
17. Ishiyama, K.; Ohdan, H.; Ohira, M.; Mitsuta, H.; Arihiro, K.; Asahara, T. Difference in cytotoxicity against hepatocellular carcinoma between liver and periphery natural killer cells in humans. Hepatology 43(2):362-372; 2006.
18. Jonsson, J. R.; Hogan, P. G.; Balderson, G. A.; Ooi, L. L.; Lynch, S. V.; Strong, R. W.; Powell, E. E. Human liver transplant perfusate: An abundant source of donor liver-associated leukocytes. Hepatology 26(5):1111-1114; 1997.
19. Kaplan, D. H.; Shankaran, V.; Dighe, A. S.; Stockert, E.; Aguet, M.; Old, L. J.; Schreiber, R. D. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA 95(13):7556-7561; 1998.
20. Kim, G. G.; Donnenberg, V. S.; Donnenberg, A. D.; Gooding, W.; Whiteside, T. L. A novel multiparametric flow cytometry-based cytotoxicity assay simultaneously immunophenotypes effector cells: Comparisons to a 4 h 51Cr-release assay. J. Immunol. Methods 325(1-2):51-66; 2007.
21. Levi, D. M.; Tzakis, A. G.; Martin, P.; Nishida, S.; Island, E.; Moon, J.; Selvaggi, G.; Tekin, A.; Madrazo, B. L.; Narayanan, G.; Garcia, M.; Feun, L.; Tryphonopoulos, P.; Skartsis, N.; Livingstone, A. Liver transplantation for hepatocellular carcinoma in the model for end-stage liver disease era. J. Am. Coll. Surg. 210(5):727-736; 2010.
22. Mandelboim, O.; Malik, P.; Davis, D. M.; Jo, C. H.; Boyson, J. E.; Strominger, J. L. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc. Natl. Acad. Sci. USA 96(10):5640-5644; 1999.
23. Mazzaferro, V.; Regalia, E.; Doci, R.; Andreola, S.; Pulvirenti, A.; Bozzetti, F.; Montalto, F.; Ammatuna, M.; Morabito, A.; Gennari, L. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N. Engl. J. Med. 334(11):693-699; 1996.
24. Miller, J. S.; Soignier, Y.; Panoskaltsis-Mortari, A.; McNearney, S. A.; Yun, G. H.; Fautsch, S. K.; McKenna, D.; Le, C.; Defor, T. E.; Burns, L. J.; Orchard, J.; Blazar, B.; Wagner, J.; Slungaard, A.; Weisdorf, D.; Okazaki, J.; McGlave, P. Successful adoptive transfer and in vivo expansion of human haploidentical natural killer (NK) cells in patients with cancer. Blood 105(8):3051-3057; 2005.
25. Moroso, V.; Metselaar, H. J.; Mancham, S.; Tilanus, H. W.; Eissens, D.; van der Meer, A.; van der Laan, L. J.; Kuipers, E. J.; Joosten, I.; Kwekkeboom, J. Liver grafts contain a unique subset of natural killer cells that are transferred into the recipient after liver transplantation. Liver Transpl. 16(7):895-908; 2010.
26. Norris, S.; Collins, C.; Doherty, D. G.; Smith, F.; McEntee, G.; Traynor, O.; Nolan, N.; Hegarty, J.; O'Farrelly, C. Resident human hepatic lymphocytes are phenotypically different from circulating lymphocytes. J. Hepatol. 28(1): 84-90; 1998.
27. Ohira, M.; Ishiyama, K.; Tanaka, Y.; Doskali, M.; Igarashi, Y.; Tashiro, H.; Hiraga, N.; Imamura, M.; Sakamoto, N.; Asahara, T.; Chayama, K.; Ohdan, H. Adoptive immunotherapy with liver allograft-derived lymphocytes induces anti-hepatitis C virus (HCV) activity after liver transplantation in humans and humanized mice. J. Clin. Invest. 119(11):3226-3235; 2009.
28. Ohira, M.; Ohdan, H.; Mitsuta, H.; Ishiyama, K.; Tanaka, Y.; Igarashi, Y.; Asahara, T. Adoptive transfer of tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-expressing natural killer cells prevents recurrence of hepatocellular carcinoma after partial hepatec-tomy. Transplantation 82(12):1712-1719; 2006.
29. Passweg, J. R.; Tichelli, A.; Meyer-Monard, S.; Heim, D.; Stern, M.; Kuhne, T.; Favre, G.; Gratwohl, A. Purified donor natural killer (NK)-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia 18(11):1835-1838; 2004.
30. Pitti, R. M.; Marsters, S. A.; Ruppert, S.; Donahue, C. J.; Moore, A.; Ashkenazi, A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271(22):12687-12690; 1996.
31. Ruggeri, L.; Mancusi, A.; Capanni, M.; Martelli, M. F.; Velardi, A. Exploitation of alloreactive natural killer (NK) cells in adoptive immunotherapy of cancer. Curr. Opin. Immunol. 17(2):211-217; 2005.
32. Saab, S.; Yeganeh, M.; Nguyen, K.; Durazo, F.; Han, S.; Yersiz, H.; Farmer, D. G.; Goldstein, L. I.; Tong, M. J.; Busuttil, R. W. Recurrence of hepatocellular carcinoma and hepatitis B reinfection in hepatitis B surface antigen-positive patients after liver transplantation. Liver Transpl. 15(11):1525-1534; 2009.
33. Schroder, K.; Hertzog, P. J.; Ravasi, T.; Hume, D. A. Interferon-gamma: An overview of signals, mechanisms and functions. J. Leukoc. Biol. 75(2):163-189; 2004.
34. Schulze, A.; Schirutschke, H.; Oelschlagel, U.; Schmitz, M.; Fussel, M.; Wassmuth, R.; Ehninger, G.; Bornhauser, M.; Platzbecker, U. Altered phenotype of natural killer cell subsets after haploidentical stem cell transplantation. Exp. Hematol. 36(4):378-389; 2008.
35. Soderdahl, G.; Backman, L.; Isoniemi, H.; Cahlin, C.; Hockerstedt, K.; Broome, U.; Makisalo, H.; Friman, S.; Ericzon, B. G. A prospective, randomized, multi-centre trial of systemic adjuvant chemotherapy versus no additional treatment in liver transplantation for hepatocellular carcinoma. Transpl. Int. 19(4):288-294; 2006.
36. Telerman, A.; Amson, R. B.; Romasco, F.; Wybran, J.; Galand, P.; Mosselmans, R. Internalization of human T lymphocyte receptors. Eur. J. Immunol. 17(7):991-997; 1987.
37. Tharavanij, T.; Froud, T.; Leitao, C. B.; Baidal, D. A.; Paz-Pabon, C. N.; Shari, M.; Cure, P.; Bernetti, K.; Ricordi, C.; Alejandro, R. Clinical use of fructosamine in islet transplantation. Cell Transplant. 18(4):453-458; 2009.
38. Trinchieri, G. Biology of natural killer cells. Adv. Immunol. 47:187-376; 1989.
39. Van Wauwe, J. P.; De Mey, J. R.; Goossens, J. G. OKT3: a monoclonal anti-human T lymphocyte antibody with potent mitogenic properties. J. Immunol. 124(6):2708-2713; 1980.
40. Vitale, M.; Bottino, C.; Sivori, S.; Sanseverino, L.; Castriconi, R.; Marcenaro, E.; Augugliaro, R.; Moretta, L.; Moretta, A. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J. Exp. Med. 187(12):2065-2072; 1998.
41. Vivarelli, M.; Cucchetti, A.; La Barba, G.; Ravaioli, M.; Del Gaudio, M.; Lauro, A.; Grazi, G. L.; Pinna, A. D. Liver transplantation for hepatocellular carcinoma under calcineurin inhibitors: Reassessment of risk factors for tumor recurrence. Ann. Surg. 248(5):857-862; 2008.
42. Vujanovic, N. L.; Nagashima, S.; Herberman, R. B.; Whiteside, T. L. Nonsecretory apoptotic killing by human natural killer (NK) cells. J. Immunol. 157(3):1117-1126; 1996.
43. Walczak, H.; Miller, R. E.; Ariail, K.; Gliniak, B.; Griffith, T. S.; Kubin, M.; Chin, W.; Jones, J.; Woodward, A.; Le, T.; Smith, C.; Smolak, P.; Goodwin, R.; Rauch, C.; Schuh, J.; Lynch, D. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5(2):157-163; 1999.
44. Wiley, S. R.; Schooley, K.; Smolak, P. J.; Din, W. S.; Huang, C. P.; Nicholl, J. K.; Sutherland, G. R.; Smith, T. D.; Rauch, C.; Smith, C. A.; Goodwin, R. Identification and characterization of a new member of the tumor necrosis factor (TNF) family that induces apoptosis. Immunity 3(6):673-682; 1995.
45. Wilson, C. H.; Stansby, G.; Haswell, M.; Cunningham, A. C.; Talbot, D. Evaluation of eight preservation solutions for endothelial in situ preservation. Transplantation 78(7):1008-1013; 2004.
46. Yokoyama, I.; Carr, B.; Saitsu, H.; Iwatsuki, S.; Starzl, T. E. Accelerated growth rates of recurrent hepatocellular carcinoma after liver transplantation. Cancer 68(10): 2095-2100; 1991.
47. Young, H. A.; Bream, J. H. IFN-gamma: Recent advances in understanding regulation of expression, biological functions, and clinical applications. Curr. Top. Microbiol. Immunol. 316:97-117; 2007.
48. Zimmerman, M. A.; Ghobrial, R. M.; Tong, M. J.; Hiatt, J. R.; Cameron, A. M.; Hong, J.; Busuttil, R. W. Recurrence of hepatocellular carcinoma following liver transplantation: A review of preoperative and postoperative prognostic indicators. Arch. Surg. 143(2):182-188; 2008.