Clinical grade purification and expansion of NK cell products for an optimized manufacturing protocol

Frontiers in Oncology

Volumn 3 MAY, Issue , 2013, Pages

  Koehl, Ulrike ^a   Brehm, Claudia ^b   Huenecke, Sabine ^b   Zimmermann, Stefanie Yvonne ^b   Kloess, Stephan ^a   Bremm, Melanie ^b   Ullrich, Evelyn ^b   Soerensen, Jan ^b   Quaiser, Andrea ^b   Erben, Stephanie ^b   Wunram, Claudia ^b   Gardlowski, Tanja ^a   Auth, Eileen ^a,b   Tonn, Torsten ^c   Seidl, Christian ^c   Meyer Monard, Sandrine ^d   Stern, Martin ^d   Passweg, Jakob ^d   Klingebiel, Thomas ^b   Bader, Peter ^b   Schwabe, Dirk ^b   Esser, Ruth ^a   more..

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c Red Cross Blood Donor Center   (Germany)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Cytotoxicity; IL 2 activation; NK cell expansion; NK cell purification; T cell removal

Indexed keywords

CD56 ANTIGEN; CD69 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN KINASE B; STAT3 PROTEIN;

ADULT; APHERESIS; ARTICLE; CELL ACTIVATION; CELL EXPANSION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; FLOW CYTOMETRY; GENOTYPING TECHNIQUE; HLA TYPING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MALE; MONOCYTE; NATURAL KILLER CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); POLYMERASE CHAIN REACTION; PURIFICATION; T CELL DEPLETION;

EID: 84891101533     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00118     Document Type: Article

References (42)

1. Becker, S., Tonn, T., Fussel, T., Uhrberg, M., Bogdanow, M., Seifried, E., et al. (2003). Assessment of killer cell immunoglobulinlike receptor expression and corresponding HLA class I phenotypes demonstrates heterogenous KIR expression independent of anticipated HLA class I ligands. Hum. Immunol. 64, 183-193.
2. Brehm, C., Huenecke, S., Quaiser, A., Esser, R., Bremm, M., Kloess, S., et al. (2011). IL-2 stimulated but not unstimulated NK cells induce selective disappearance of peripheral blood cells: concomitant results to a phase I/II study. PLoS ONE 6:e27351. doi:10.1371/journal.pone.0027351
3. Curti, A., Ruggeri, L., D'Addio, A., Bontadini, A., Dan, E., Motta, M. R., et al. (2011). Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood 118, 3273-3279.
4. Esser, R., Muller, T., Stefes, D., Kloess, S., Seidel, D., Gillies, S. D., et al. (2012). NK cells engineered to express a GD2-specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J. Cell. Mol. Med. 16, 569-581.
5. Farag, S. S., Fehniger, T. A., Ruggeri, L., Velardi, A., and Caligiuri, M. A. (2002). Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood 100, 1935-1947.
6. Heinze, A., Elze, M. C., Kloess, S., Ciocarlie, O., Konigs, C., Betz, S., et al. (2013). Age-matched dendritic cell subpopulations reference values in childhood. Scand. J. Immunol. 77, 213-220.
7. Huenecke, S., Zimmermann, S. Y., Kloess, S., Esser, R., Brinkmann, A., Tramsen, L., et al. (2010). IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16-subpopulations and in vivo influence after haploidentical NK cell infusion. J. Immunother. 33, 200-210.
8. Iyengar, R., Handgretinger, R., Babarin-Dorner, A., Leimig, T., Otto, M., Geiger, T. L., et al. (2003). Purification of human natural killer cells using a clinical-scale immunomagnetic method. Cytotherapy 5, 479-484.
9. Jacobs, B., and Ullrich, E. (2012). The interaction of NK cells and dendritic cells in the tumor environment: how to enforce NK cell & DC action under immunosuppressive conditions? Curr. Med. Chem. 19, 1771-1779.
10. Keeney, M., Chin-Yee, I., Weir, K., Popma, J., Nayar, R., and Sutherland, D. R. (1998). Single platform flow cytometric absolute CD34+ cell counts based on the ISHAGE guidelines. International Society of Hematotherapy and Graft Engineering. Cytometry 34, 61-70.
11. Kloess, S., Huenecke, S., Piechulek, D., Esser, R., Koch, J., Brehm, C., et al. (2010). IL-2-activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuroblastoma patients by scavenging of plasma MICA. Eur. J. Immunol. 40, 3255-3267.
12. Kloss, S., Bochennek, K., Huenecke, S., Zimmermann, S. Y., Kuci, S., Muller, T., et al. (2007). A novel five-colour flow cytometric assay to determine NK cell cytotoxicity against neuroblastoma and other adherent tumour cells. J. Immunol. Methods 325, 140-147.
13. Koehl, U., Bochennek, K., Esser, R., Brinkmann, A., Quaritsch, R., Becker, M., et al. (2008). ISHAGE-based single-platform flowcytometric analysis for measurement of absolute viable T cells in fresh or cryopreserved products: CD34/CD133 selected or CD3/CD19 depleted stem cells, DLI and purified CD56+CD3-NK cells. Int. J. Hematol. 87, 98-105.
14. Koehl, U., Esser, R., Zimmermann, S., Tonn, T., Kotchetkov, R., Bartling, T., et al. (2005). Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin. Padiatr. 217, 345-350.
15. Koehl, U., Sorensen, J., Esser, R., Zimmermann, S., Gruttner, H. P., Tonn, T., et al. (2004). IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol. Dis. 33, 261-266.
16. Koepsell, S. A., Miller, J. S., and McKenna, D. H. Jr. (2013). Natural killer cells: a review of manufacturing and clinical utility. Transfusion 53, 404-410.
17. Lang, P., Handgretinger, R., Niethammer, D., Schlegel, P. G., Schumm, M., Greil, J., et al. (2003). Transplantation of highly purified CD34+ progenitor cells from unrelated donors in pediatric leukemia. Blood 101, 1630-1636.
18. Lanier, L. L. (2005). NK cell recognition. Annu. Rev. Immunol. 23, 225-274.
19. Lapteva, N., Durett, A. G., Sun, J., Rollins, L. A., Huye, L. L., Fang, J., et al. (2012). Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. Cytotherapy 14, 1131-1143.
20. Ljunggren, H. G., and Malmberg, K. J. (2007). Prospects for the use of NK cells in immunotherapy of human cancer. Nat. Rev. Immunol. 7, 329-339.
21. McKenna, D. H. Jr., Sumstad, D., Bostrom, N., Kadidlo, D. M., Fautsch, S., McNearney, S., et al. (2007). Good manufacturing practices production of natural killer cells for immunotherapy: a six-year single-institution experience. Transfusion 47, 520-528.
22. McKenna, D. H., Kadidlo, D. M., Cooley, S., and Miller, J. S. (2012). Clinical production and therapeutic applications of alloreactive natural killer cells. Methods Mol. Biol. 882, 491-507.
23. Meyer-Monard, S., Passweg, J., Siegler, U., Kalberer, C., Koehl, U., Rovo, A., et al. (2009). Clinical-grade purification of natural killer cells in haploidentical hematopoietic stem cell transplantation. Transfusion 49, 362-371.
24. Miller, J. S., Soignier, Y., Panoskaltsis-Mortari, A., McNearney, S. A., Yun, G. H., Fautsch, S. K., et al. (2005). Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105, 3051-3057.
25. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., et al. (2001). Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19, 197-223.
26. Nguyen, S., Beziat, V., Norol, F., Uzunov, M., Trebeden-Negre, H., Azar, N., et al. (2011). Infusion of allogeneic natural killer cells in a patient with acute myeloid leukemia in relapse after haploidentical hematopoietic stem cell transplantation. Transfusion 51, 1769-1778.
27. Obeidy, P., and Sharland, A. F. (2009). NKG2D and its ligands. Int. J. Biochem. Cell Biol. 41, 2364-2367.
28. Pallandre, J. R., Krzewski, K., Bedel, R., Ryffel, B., Caignard, A., Rohrlich, P. S., et al. (2008). Dendritic cell and natural killer cell cross-talk: a pivotal role of CX3CL1 in NK cytoskeleton organization and activation. Blood 112, 4420-4424.
29. Passweg, J. R., Koehl, U., Uharek, L., Meyer-Monard, S., and Tichelli, A. (2006). Natural-killer-cell-based treatment in haematopoietic stem-cell transplantation. Best Pract. Res. Clin. Haematol. 19, 811-824.
30. Passweg, J. R., Tichelli, A., Meyer-Monard, S., Heim, D., Stern, M., Kuhne, T., et al. (2004). Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia 18, 1835-1838.
31. Rizzieri, D. A., Storms, R., Chen, D. F., Long, G., Yang, Y., Nikcevich, D. A., et al. (2010). Natural killer cell-enriched donor lymphocyte infusions from A 3-6/6 HLA matched family member following nonmyeloablative allogeneic stem cell transplantation. Biol. Blood Marrow Transplant. 16, 1107-1114.
32. Rubnitz, J. E., Inaba, H., Ribeiro, R. C., Pounds, S., Rooney, B., Bell, T., et al. (2010). NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J. Clin. Oncol. 28, 955-959.
33. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., et al. (2002). Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295, 2097-2100.
34. Shook, D. R., and Campana, D. (2011). Natural killer cell engineering for cellular therapy of cancer. Tissue Antigens 78, 409-415.
35. Siegler, U., Meyer-Monard, S., Jorger, S., Stern, M., Tichelli, A., Gratwohl, A., et al. (2010). Good manufacturing practice-compliant cell sorting and large-scale expansion of single KIR-positive alloreactive human natural killer cells for multiple infusions to leukemia patients. Cytotherapy 12, 750-763.
36. Spanholtz, J., Tordoir, M., Eissens, D., Preijers, F., van der Meer, A., Joosten, I., et al. (2010). High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PLoS ONE 5:e9221. doi:10.1371/journal.pone.0009221
37. Stern, M., Passweg, J. R., Meyer-Monard, S., Esser, R., Tonn, T., Soerensen, J., et al. (2013). Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant. 48, 433-438.
38. Sutlu, T., Stellan, B., Gilljam, M., Quezada, H. C., Nahi, H., Gahrton, G., et al. (2010). Clinical-grade, large-scale, feeder-free expansion of highly active human natural killer cells for adoptive immunotherapy using an automated bioreactor. Cytotherapy 12, 1044-1055.
39. Vivier, E., Ugolini, S., Blaise, D., Chabannon, C., and Brossay, L. (2012). Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol. 12, 239-252.
40. Walzer, T., Dalod, M., Vivier, E., and Zitvogel, L. (2005). Natural killer cell-dendritic cell crosstalk in the initiation of immune responses. Expert Opin. Biol. Ther. 5(Suppl. 1), S49-59.
41. Wehner, R., Lobel, B., Bornhauser, M., Schakel, K., Cartellieri, M., Bachmann, M., et al. (2009). Reciprocal activating interaction between 6-sulfo LacNAc+ dendritic cells and NK cells. Int. J. Cancer 124, 358-366.
42. Zimmermann, S. Y., Esser, R., Rohrbach, E., Klingebiel, T., and Koehl, U. (2005). A novel four-colour flow cytometric assay to determine natural killer cell or T-cell-mediated cellular cytotoxicity against leukaemic cells in peripheral or bone marrow specimens containing greater than 20% of normal cells. J. Immunol. Methods 296, 63-76.