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Evaluation of therapeutic effects of natural killer (NK) cell-based immunotherapy in mice using in vivo apoptosis bioimaging with a caspase-3 sensor

dc.contributor.authorLee, Ho Won
dc.contributor.authorSingh, Thoudam Debraj
dc.contributor.authorLee, Sang‐woo
dc.contributor.authorHa, Jeoung‐hee
dc.contributor.authorRehemtulla, Alnawaz
dc.contributor.authorAhn, Byeong‐cheol
dc.contributor.authorJeon, Young Hyun
dc.contributor.authorLee, Jaetae
dc.date.accessioned2020-03-17T18:35:44Z
dc.date.available2020-03-17T18:35:44Z
dc.date.issued2014-07
dc.identifier.citationLee, Ho Won; Singh, Thoudam Debraj; Lee, Sang‐woo ; Ha, Jeoung‐hee ; Rehemtulla, Alnawaz; Ahn, Byeong‐cheol ; Jeon, Young Hyun; Lee, Jaetae (2014). "Evaluation of therapeutic effects of natural killer (NK) cellâ based immunotherapy in mice using in vivo apoptosis bioimaging with a caspaseâ 3 sensor." The FASEB Journal 28(7): 2932-2941.
dc.identifier.issn0892-6638
dc.identifier.issn1530-6860
dc.identifier.urihttps://hdl.handle.net/2027.42/154541
dc.description.abstractNatural killer (NK) cellâ based immunotherapy is a promising strategy for cancer treatment, and caspaseâ 3 is an important effector molecule in NK cellâ mediated apoptosis in cancers. Here, we evaluated the antitumor effects of NK cellâ based immunotherapy by serial noninvasive imaging of apoptosis using a caspaseâ 3 sensor in mice with human glioma xenografts. Human glioma cells expressing both a caspaseâ 3 sensor as a surrogate marker for caspaseâ 3 activation and Renilla luciferase (Rluc) as a surrogate marker for cell viability were established and referred to as D54â CR cells. Human NK92 cells were used as effector cells. Treatment with NK92 cells resulted in a timeâ and effector numberâ dependent increase in bioluminescence imaging (BLI) activity of the caspaseâ 3 sensor in D54â CR cells in vitro. Caspaseâ 3 activation by NK92 treatment was blocked by Zâ VAD treatment in D54â CR cells. Transfusion of NK92 cells induced an increase of the BLI signal by caspaseâ 3 activation in a doseâ and timeâ dependent manner in D54â CR tumorâ bearing mice but not in PBSâ treated mice. Accordingly, sequential BLI with the Rluc reporter gene revealed marked retardation of tumor growth in the NK92â treatment group but not in the PBSâ treatment group. These data suggest that noninvasive imaging of apoptosis with a caspaseâ 3 sensor can be used as an effective tool for evaluation of therapeutic efficacy as well as for optimization of NK cellâ based immunotherapy.â Lee, H. W., Singh, T. D., Lee, S.â W., Ha, J.â H., Rehemtulla, A., Ahn, B.â C., Jeon, Y.â H., Lee, J. Evaluation of therapeutic effects of natural killer (NK) cellâ based immunotherapy in mice using in vivo apoptosis bioimaging with a caspaseâ 3 sensor. FASEB J. 28, 2932â 2941 (2014). www.fasebj.org
dc.publisherWiley Periodicals, Inc.
dc.publisherFederation of American Societies for Experimental Biology
dc.subject.otherRenilla luciferase
dc.subject.otherglioma
dc.subject.othermolecular imaging
dc.titleEvaluation of therapeutic effects of natural killer (NK) cell-based immunotherapy in mice using in vivo apoptosis bioimaging with a caspase-3 sensor
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelBiology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/154541/1/fsb2fj13243014.pdf
dc.identifier.doi10.1096/fj.13-243014
dc.identifier.sourceThe FASEB Journal
dc.identifier.citedreferenceReefman, E., Kay, J. G., Wood, S. M., Offenhauser, C., Brown, D. L., Roy, S., Stanley, A. C., Low, P. C., Manderson, A. P., and Stow, J. L. ( 2010 ) Cytokine secretion is distinct from secretion of cytotoxic granules in NK cells. J. Immunol. 184, 4852 â 4862
dc.identifier.citedreferenceLanier, L. L. ( 2008 ) Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 8, 259 â 268
dc.identifier.citedreferenceRosen, D., Li, J. H., Keidar, S., Markon, I., Orda, R., and Berke, G. ( 2000 ) Tumor immunity in perforin-deficient mice: a role for CD95 (Fas/APO-1). J. Immunol. 164, 3229 â 3235
dc.identifier.citedreferenceTrapani, J. A., and Smyth, M. J. ( 2002 ) Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2, 735 â 747
dc.identifier.citedreferenceScrepanti, V., Wallin, R. P., Grandien, A., and Ljunggren, H. G. ( 2005 ) Impact of FASL-induced apoptosis in the elimination of tumor cells by NK cells. Mol. Immunol. 42, 495 â 499
dc.identifier.citedreferenceMcQueen, K. L., and Parham, P. ( 2002 ) Variable receptors controlling activation and inhibition of NK cells. Curr. Opin. Immunol. 14, 615 â 621
dc.identifier.citedreferenceShi, J., Tricot, G. J., Garg, T. K., Malaviarachchi, P. A., Szmania, S. M., Kellum, R. E., Storrie, B., Mulder, A., Shaughnessy, J. D. Jr., Barlogie, B., and van Rhee, F. ( 2008 ) Bortezomib down-regulates the cell-surface expression of HLA class I and enhances natural killer cell-mediated lysis of myeloma. Blood 111, 1309 â 1317
dc.identifier.citedreferenceZamai, L., Ponti, C., Mirandola, P., Gobbi, G., Papa, S., Galeotti, L., Cocco, L., and Vitale, M. ( 2007 ) NK cells and cancer. J. Immunol. 178, 4011 â 4016
dc.identifier.citedreferenceKepp, O., Galluzzi, L., Lipinski, M., Yuan, J., and Kroemer, G. ( 2011 ) Cell death assays for drug discovery. Nat. Rev. Drug Discov. 10, 221 â 237
dc.identifier.citedreferenceCoppola, J. M., Ross, B. D., and Rehemtulla, A. ( 2008 ) Noninvasive imaging of apoptosis and its application in cancer therapeutics. Clin. Cancer Res. 14, 2492 â 2501
dc.identifier.citedreferenceTerme, M., Ullrich, E., Delahaye, N. F., Chaput, N., and Zitvogel, L. ( 2008 ) Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat. Immunol. 9, 486 â 494
dc.identifier.citedreferenceYan, Y., Steinherz, P., Klingemann, H. G., Dennig, D., Childs, B. H., McGuirk, J., and O’Reilly, R. J. ( 1998 ) Antileukemia activity of a natural killer cell line against human leukemias. Clin. Cancer Res. 4, 2859 â 2868
dc.identifier.citedreferenceTam, Y. K., Martinson, J. A., Doligosa, K., and Klingemann, H. G. ( 2003 ) Ex vivo expansion of the highly cytotoxic human natural killer-92 cell-line under current good manufacturing practice conditions for clinical adoptive cellular immunotherapy. Cytotherapy 5, 259 â 272
dc.identifier.citedreferenceAshkenazi, A., Pai, R. C., Fong, S., Leung, S., Lawrence, D. A., Marsters, S. A., Blackie, C., Chang, L., McMurtrey, A. E., Hebert, A., De Forge, L., Koumenis, I. L., Lewis, D., Harris, L., Bussiere, J., Koeppen, H., Shahrokh, Z., and Schwall, R. H. ( 1999 ) Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104, 155 â 162
dc.identifier.citedreferenceLin, T., Huang, X., Gu, J., Zhang, L., Roth, J. A., Xiong, M., Curley, S. A., Yu, Y., Hunt, K. K., and Fang, B. ( 2002 ) Long-term tumor-free survival from treatment with the GFP-TRAIL fusion gene expressed from the hTERT promoter in breast cancer cells. Oncogene 21, 8020 â 8028
dc.identifier.citedreferenceJacob, D., Davis, J., Zhu, H., Zhang, L., Teraishi, F., Wu, S., Marini, F. C., 3rd, and Fang, B. ( 2004 ) Suppressing orthotopic pancreatic tumor growth with a fiber-modified adenovector expressing the TRAIL gene from the human telomerase reverse transcriptase promoter. Clin. Cancer Res. 10, 3535 â 3541
dc.identifier.citedreferenceMuller, T., Uherek, C., Maki, G., Chow, K. U., Schimpf, A., Klingemann, H. G., Tonn, T., and Wels, W. S. ( 2008 ) Expression of a CD20-specific chimeric antigen receptor enhances cytotoxic activity of NK cells and overcomes NK-resistance of lymphoma and leukemia cells. Cancer Immunol. Immunother. 57, 411 â 423
dc.identifier.citedreferenceNagashima, S., Mailliard, R., Kashii, Y., Reichert, T. E., Herberman, R. B., Robbins, P., and Whiteside, T. L. ( 1998 ) Stable transduction of the interleukin-2 gene into human natural killer cell lines and their phenotypic and functional characterization in vitro and in vivo. Blood 91, 3850 â 3861
dc.identifier.citedreferenceReid, G. S., Bharya, S., Klingemann, H. G., and Schultz, K. R. ( 2002 ) Differential killing of pre-B acute lymphoblastic leukaemia cells by activated NK cells and the NK-92 ci cell line. Clin. Exp. Immunol. 129, 265 â 271
dc.identifier.citedreferenceUherek, C., Tonn, T., Uherek, B., Becker, S., Schnierle, B., Klingemann, H. G., and Wels, W. ( 2002 ) Retargeting of natural killer-cell cytolytic activity to ErbB2-expressing cancer cells results in efficient and selective tumor cell destruction. Blood 100, 1265 â 1273
dc.identifier.citedreferenceDai, C., and Krantz, S. B. ( 1999 ) Interferon gamma induces upregulation and activation of caspases 1, 3, and 8 to produce apoptosis in human erythroid progenitor cells. Blood 93, 3309 â 3316
dc.identifier.citedreferenceNowosielska, E. M., Cheda, A., Wrembel-Wargocka, J., and Janiak, M. K. ( 2011 ) Anti-neoplastic and immunostimulatory effects of low-dose X-ray fractions in mice. Int. J. Radiat. Biol. 87, 202 â 212
dc.identifier.citedreferenceIshikawa, E., Tsuboi, K., Saijo, K., Takano, S., and Ohno, T. ( 2004 ) X-irradiation to human malignant glioma cells enhances the cytotoxicity of autologous killer lymphocytes under specific conditions. Int. J. Radiat. Oncol. Biol. Phys. 59, 1505 â 1512
dc.identifier.citedreferenceHori, T., Kondo, T., Kanamori, M., Tabuchi, Y., Ogawa, R., Zhao, Q. L., Ahmed, K., Yasuda, T., Seki, S., Suzuki, K., and Kimura, T. ( 2010 ) Ionizing radiation enhances tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis through up-regulations of death receptor 4 (DR4) and death receptor 5 (DR5) in human osteosarcoma cells. J. Orthop. Res. 28, 739 â 745
dc.identifier.citedreferenceJeon, Y. H., Choi, Y., Kim, C. W., Kim, Y. H., Youn, H., Lee, J., and Chung, J. K. ( 2010 ) Human sodium/iodide symporter-mediated radioiodine gene therapy enhances the killing activities of CTLs in a mouse tumor model. Mol. Cancer Ther. 9, 126 â 133
dc.identifier.citedreferenceRamakrishnan, R., Assudani, D., Nagaraj, S., Hunter, T., Cho, H. I., Antonia, S., Altiok, S., Celis, E., and Gabrilovich, D. I. ( 2010 ) Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J. Clin. Invest. 120, 1111 â 1124
dc.identifier.citedreferenceMelder, R. J., Brownell, A. L., Shoup, T. M., Brownell, G. L., and Jain, R. K. ( 1993 ) Imaging of activated natural killer cells in mice by positron emission tomography: preferential uptake in tumors. Cancer Res. 53, 5867 â 5871
dc.identifier.citedreferenceCerwenka, A., and Lanier, L. L. ( 2001 ) Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 1, 41 â 49
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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