Natural killer cells stimulated with PM21 particles expand and biodistribute in vivo: Clinical implications for cancer treatment

Cytotherapy

Volumn 18, Issue 5, 2016, Pages 653-663

  Oyer, Jeremiah L ^a   Pandey, Veethika ^a   Igarashi, Robert Y ^a   Somanchi, Srinivas S ^b   Zakari, Ahmed ^c   Solh, Melhem ^c   Lee, Dean A ^b   Altomare, Deborah A ^a   Copik, Alicja J ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c FLORIDA HOSPITAL CANCER INSTITUTE   (United States)

Author keywords

In vivo NK cell expansion; Membrane bound IL 21; Membrane particles; NK cells

Indexed keywords

CD137 LIGAND; CD45 ANTIGEN; INTERLEUKIN 21; RECOMBINANT INTERLEUKIN 2; INTERLEUKIN 2; INTERLEUKIN DERIVATIVE;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRAIN; CANCER IMMUNOTHERAPY; CELL ACTIVATION; CELL EXPANSION; CELL MEMBRANE; CELL STIMULATION; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MEGADOSE; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; K562 CELL LINE; LIVER; LUNG; LYMPHOCYTE COUNT; MOUSE; NATURAL KILLER CELL; NOD SCID GAMMA MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PM21 PARTICLE; PRIORITY JOURNAL; SPLEEN; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; FEMALE; IMMUNOLOGY; IMMUNOTHERAPY; K-562 CELL LINE; LEUKEMIA, MYELOID, ACUTE; LYMPHOCYTE ACTIVATION; MALE; MONONUCLEAR CELL; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CELL PROLIFERATION; FEMALE; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-2; INTERLEUKINS; K562 CELLS; KILLER CELLS, NATURAL; LEUKEMIA, MYELOID, ACUTE; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED NOD; MICE, SCID;

EID: 84962046512     PISSN: 14653249     EISSN: 14772566     Source Type: Journal    
DOI: 10.1016/j.jcyt.2016.02.006     Document Type: Article

References (38)

1. Klingemann H.G. Cellular therapy of cancer with natural killer cells-where do we stand?. Cytotherapy 2013, 15:1185-1194.
2. Knorr D.A., Bachanova V., Verneris M.R., Miller J.S. Clinical utility of natural killer cells in cancer therapy and transplantation. Semin Immunol 2014, 26:161-172.
3. West W.H., Tauer K.W., Yannelli J.R., Marshall G.D., Orr D.W., Thurman G.B., et al. Constant-infusion recombinant interleukin-2 in adoptive immunotherapy of advanced cancer. N Engl J Med 1987, 316:898-905.
4. Miller J.S., Soignier Y., Panoskaltsis-Mortari A., McNearney S.A., Yun G.H., Fautsch S.K., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005, 105:3051-3057.
5. Leclercq G., Debacker V., de Smedt M., Plum J. Differential effects of interleukin-15 and interleukin-2 on differentiation of bipotential T/natural killer progenitor cells. J Exp Med 1996, 184:325-336.
6. Rodella L., Zamai L., Rezzani R., Artico M., Peri G., Falconi M., et al. Interleukin 2 and interleukin 15 differentially predispose natural killer cells to apoptosis mediated by endothelial and tumour cells. Br J Haematol 2001, 115:442-450.
7. Ross M.E., Caligiuri M.A. Cytokine-induced apoptosis of human natural killer cells identifies a novel mechanism to regulate the innate immune response. Blood 1997, 89:910-918.
8. Dijkers P.F., Birkenkamp K.U., Lam E.W., Thomas N.S., Lammers J.W., Koenderman L., et al. FKHR-L1 can act as a critical effector of cell death induced by cytokine withdrawal: protein kinase B-enhanced cell survival through maintenance of mitochondrial integrity. J Cell Biol 2002, 156:531-542.
9. Berg M., Lundqvist A., McCoy P., Samsel L., Fan Y., Tawab A., et al. Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy 2009, 11:341-355.
10. Park K.U., Jin P., Sabatino M., Feng J., Civini S., Khuu H., et al. Gene expression analysis of ex vivo expanded and freshly isolated NK cells from cancer patients. J Immunother 2010, 33:945-955.
11. Fujisaki H., Kakuda H., Shimasaki N., Imai C., Ma J., Lockey T., et al. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res 2009, 69:4010-4017.
12. Denman C.J., Senyukov V.V., Somanchi S.S., Phatarpekar P.V., Kopp L.M., Johnson J.L., et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS ONE 2012, 7:e30264.
13. Romee R., Foley B., Lenvik T., Wang Y., Zhang B., Ankarlo D., et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 2013, 121:3599-3608.
14. Somanchi S.S., Senyukov V.V., Denman C.J., Lee D.A. Expansion, purification, and functional assessment of human peripheral blood NK cells. J Vis Exp 2011, (48). 10.3791/2540.
15. Childs R.W., Carlsten M. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat Rev Drug Discov 2015, 14(7):487-498.
16. Miller J.S. Should natural killer cells be expanded in vivo or ex vivo to maximize their therapeutic potential?. Cytotherapy 2009, 11:259-260.
17. Oyer J.L., Igarashi R.Y., Kulikowski A.R., Colosimo D.A., Solh M.M., Zakari A., et al. Generation of highly cytotoxic natural killer cells for treatment of acute myelogenous leukemia using a feeder-free, particle-based approach. Biol Blood Marrow Transplant 2015, 21:632-639.
18. Miller J.S., Rooney C.M., Curtsinger J., McElmurry R., McCullar V., Verneris M.R., et al. Expansion and homing of adoptively transferred human natural killer cells in immunodeficient mice varies with product preparation and in vivo cytokine administration: implications for clinical therapy. Biol Blood Marrow Transplant 2014, 20:1252-1257.
19. Geller M.A., Knorr D.A., Hermanson D.A., Pribyl L., Bendzick L., McCullar V., et al. Intraperitoneal delivery of human natural killer cells for treatment of ovarian cancer in a mouse xenograft model. Cytotherapy 2013, 15:1297-1306.
20. Cany J., van der Waart A.B., Tordoir M., Franssen G.M., Hangalapura B.N., de Vries J., et al. Natural killer cells generated from cord blood hematopoietic progenitor cells efficiently target bone marrow-residing human leukemia cells in NOD/SCID/IL2Rg(null) mice. PLoS ONE 2013, 8:e64384.
21. + NK cell expansion. J Clin Invest 2014, 124:5305-5316.
22. Foley B., Cooley S., Verneris M.R., Pitt M., Curtsinger J., Luo X., et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012, 119:2665-2674.
23. Foley B., Cooley S., Verneris M.R., Curtsinger J., Luo X., Waller E.K., et al. Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol 2012, 189:5082-5088.
24. Davis Z.B., Cooley S.A., Cichocki F., Felices M., Wangen R., Luo X., et al. Adaptive natural killer cell and killer cell immunoglobulin-like receptor-expressing T cell responses are induced by cytomegalovirus and are associated with protection against cytomegalovirus reactivation after allogeneic donor hematopoietic cell transplantation. Biol Blood Marrow Transplant 2015, 21:1653-1662.
25. Sarkar S., van Gelder M., Noort W., Xu Y., Rouschop K.M., Groen R., et al. Optimal selection of natural killer cells to kill myeloma: the role of HLA-E and NKG2A. Cancer Immunol Immunother 2015, 64:941-963.
26. Carlsten M., Childs R.W. Genetic manipulation of NK cells for cancer Immunotherapy: techniques and clinical implications. Front Immunol 2015, 6:266.
27. Phan T.G., Long G.V., Scolyer R.A. Checkpoint inhibitors for cancer immunotherapy. Multiple checkpoints on the long road towards cancer immunotherapy. Immunol Cell Biol 2015, 93:323-325.
28. Glienke W., Esser R., Priesner C., Suerth J.D., Schambach A., Wels W.S., et al. Advantages and applications of CAR-expressing natural killer cells. Front Pharmacol 2015, 6:21.
29. Chang Y.H., Connolly J., Shimasaki N., Mimura K., Kono K., Campana D. A chimeric receptor with NKG2D specificity enhances natural killer cell activation and killing of tumor cells. Cancer Res 2013, 73:1777-1786.
30. Shimasaki N., Fujisaki H., Cho D., Masselli M., Lockey T., Eldridge P., et al. A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy 2012, 14:830-840.
31. Altvater B., Landmeier S., Pscherer S., Temme J., Schweer K., Kailayangiri S., et al. 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin Cancer Res 2009, 15:4857-4866.
32. + targets. Blood 2014, 123:3016-3026.
33. Bachanova V., Cooley S., Defor T.E., Verneris M.R., Zhang B., McKenna D.H., et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood 2014, 123:3855-3863.
34. Zhu E.F., Gai S.A., Opel C.F., Kwan B.H., Surana R., Mihm M.C., et al. Synergistic innate and adaptive immune response to combination immunotherapy with anti-tumor antigen antibodies and extended serum half-life IL-2. Cancer Cell 2015, 27:489-501.
35. Nguyen S., Kuentz M., Vernant J.P., Dhedin N., Bories D., Debre P., et al. Involvement of mature donor T cells in the NK cell reconstitution after haploidentical hematopoietic stem-cell transplantation. Leukemia 2008, 22:344-352.
36. Fehniger T.A., Cooper M.A., Nuovo G.J., Cella M., Facchetti F., Colonna M., et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003, 101:3052-3057.
37. Kohrt H.E., Thielens A., Marabelle A., Sagiv-Barfi I., Sola C., Chanuc F., et al. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood 2014, 123:678-686.
38. Romagne F., Andre P., Spee P., Zahn S., Anfossi N., Gauthier L., et al. Preclinical characterization of 1-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood 2009, 114:2667-2677.