Evaluating natural killer cell cytotoxicity against solid tumors using a microfluidic model

References

• Im A, Pavletic SZ. Immunotherapy in hematologic malignancies: past, present, and future. J Hematol Oncol. 2017;10:94. doi:10.1186/s13045-017-0453-8.
   PubMed Web of Science ®Google Scholar
• Jeanbart L, Swartz MA. Engineering opportunities in cancer immunotherapy. Proc Natl Acad Sci USA. 2015;112:14467–14472. doi:10.1073/pnas.1508516112.
   PubMed Web of Science ®Google Scholar
• June CH, O’Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science. 2018;359:1361–1365. doi:10.1126/science.aar6711.
   PubMed Web of Science ®Google Scholar
• Sahin U, Tureci O. Personalized vaccines for cancer immunotherapy. Science. 2018;359:1355–1360. doi:10.1126/science.aar7112.
   PubMed Web of Science ®Google Scholar
• Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359:1350–1355. doi:10.1126/science.aar4060.
   PubMed Web of Science ®Google Scholar
• Stagg J, Smyth MJ. NK cell-based cancer immunotherapy. Drug News Perspect. 2007;20:155–163. doi:10.1358/dnp.2007.20.3.1092096.
   PubMedGoogle Scholar
• Ye B, Stary CM, Gao Q, Wang Q, Zeng Z, Jian Z, Gu L, Xiong X. Genetically modified T-Cell-Based adoptive immunotherapy in hematological malignancies. J Immunol Res. 2017;2017:5210459. doi:10.1155/2017/5974574.
   PubMedGoogle Scholar
• Paul S, Lal G. The molecular mechanism of natural killer cells function and its importance in cancer immunotherapy. Front Immunol. 2017;8. doi:10.3389/fimmu.2017.01124.
   Web of Science ®Google Scholar
• Kohrt HE, Houot R, Marabelle A, Cho HJ, Osman K, Goldstein M, Levy R, Brody J. Combination strategies to enhance antitumor ADCC. Immunotherapy-Uk. 2012;4:511–527. doi:10.2217/imt.12.38.
   PubMed Web of Science ®Google Scholar
• Wang W, Erbe AK, Hank JA, Morris ZS, Sondel PM. NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy. Front Immunol. 2015;6. doi:10.3389/fimmu.2015.00368.
   Web of Science ®Google Scholar
• Pitt JM, Marabelle A, Eggermont A, Soria JC, Kroemer G, Zitvogel L. Targeting the tumor microenvironment: removing obstruction to anticancer immune responses and immunotherapy. Ann Oncol. 2016;27:1482–1492. doi:10.1093/annonc/mdw168.
   PubMed Web of Science ®Google Scholar
• Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39:1–10. doi:10.1016/j.immuni.2013.07.012.
   PubMed Web of Science ®Google Scholar
• Mgrditchian T, Arakelian T, Paggetti J, Noman MZ, Viry E, Moussay E, Van Moer K, Kreis S, Guerin C, Buart S, et al. Targeting autophagy inhibits melanoma growth by enhancing NK cells infiltration in a CCL5-dependent manner. Proc Natl Acad Sci USA. 2017;114:E9271–E9. doi:10.1073/pnas.1703921114.
   PubMed Web of Science ®Google Scholar
• Sandel MH, Speetjens FM, Menon AG, Albertsson PA, Basse PH, Hokland M, Nagelkerke JF, Tollenaar RAEM, van de Velde CJH, Kuppen PJK. Natural killer cells infiltrating colorectal cancer and MHC class I expression. Mol Immunol. 2005;42:541–546. doi:10.1016/j.molimm.2004.07.039.
   PubMed Web of Science ®Google Scholar
• Wang B, Wang Q, Wang Z, Jiang J, Yu S-C, Ping Y-F, Yang J, Xu S-L, Ye X-Z, Xu C, et al. Metastatic consequences of immune escape from NK cell cytotoxicity by human breast cancer stem cells. Cancer Res. 2014;74:5746–5757. doi:10.1158/0008-5472.CAN-13-2563.
   PubMed Web of Science ®Google Scholar
• Levi I, Amsalem H, Nissan A, Darash-Yahana M, Peretz T, Mandelboim O, Rachmilewitz J. Characterization of tumor infiltrating natural killer cell subset. Oncotarget. 2015;6:13835–13843. doi:10.18632/oncotarget.3453.
   PubMed Web of Science ®Google Scholar
• Carmona-Fontaine C, Bucci V, Akkari L, Deforet M, Joyce JA, Xavier JB. Emergence of spatial structure in the tumor microenvironment due to the Warburg effect. Proc Natl Acad Sci USA. 2013;110:19402–19407. doi:10.1073/pnas.1311939110.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19:1423–1437. doi:10.1038/nm.3394.
   PubMed Web of Science ®Google Scholar
• Bi JC, Tian ZG. NK Cell exhaustion. Front Immunol. 2017;8. doi:10.3389/fimmu.2017.00760.
   Web of Science ®Google Scholar
• Hasmim M, Messai Y, Ziani L, Thiery J, Bouhris J-H, Noman MZ, Chouaib S. Critical role of tumor microenvironment in shaping NK cell functions: implication of hypoxic stress. Front Immunol. 2015;6. doi:10.3389/fimmu.2015.00482.
   PubMed Web of Science ®Google Scholar
• Balsamo M, Manzini C, Pietra G, Raggi F, Blengio F, Mingari MC, Varesio L, Moretta L, Bosco MC, Vitale M. Hypoxia downregulates the expression of activating receptors involved in NK-cell-mediated target cell killing without affecting ADCC. Eur J Immunol. 2013;43:2756–2764. doi:10.1002/eji.201343448.
   PubMed Web of Science ®Google Scholar
• Yamada N, Yamanegi K, Ohyama H, Hata M, Nakasho K, Futani H, Okamura H, Terada N. Hypoxia downregulates the expression of cell surface MICA without increasing soluble MICA in osteosarcoma cells in a HIF-1 alpha-dependent manner. Int J Oncol. 2012;41:2005–2012. doi:10.3892/ijo.2012.1630.
   PubMed Web of Science ®Google Scholar
• de Andrade LF, Tay RE, Pan D, Luoma AM, Ito Y, Badrinath S, Tsoucas D, Franz B, May KF, Harvey CJ, et al. Antibody-mediated inhibition of MICA and MICB shedding promotes NK cell-driven tumor immunity. Science. 2018;359:1537–1542. doi:10.1126/science.aao0505.
   PubMed Web of Science ®Google Scholar
• Carlsten M, Childs RW. Genetic manipulation of NK Cells for cancer immunotherapy: techniques and clinical implications. Front Immunol. 2015;6:266. doi:10.3389/fimmu.2015.00266.
   PubMed Web of Science ®Google Scholar
• Inngjerdingen M, Rolstad B, Ryan JC. Activating and inhibitory Ly49 receptors modulate NK cell chemotaxis to CXC chemokine ligand (CXCL) 10 and CXCL12. J Immunol. 2003;171:2889–2895.
   PubMed Web of Science ®Google Scholar
• Boissel L, Betancur M, Lu W, Wels WS, Marino T, Van Etten RA, Klingemann H. Comparison of mRNA and lentiviral based transfection of natural killer cells with chimeric antigen receptors recognizing lymphoid antigens. Leuk Lymphoma. 2012;53:958–965. doi:10.3109/10428194.2011.634048.
   PubMed Web of Science ®Google Scholar
• Binyamin L, Alpaugh RK, Hughes TL, Lutz CT, Campbell KS, Weiner LM. Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy. J Immunol. 2008;180:6392–6401.
   PubMed Web of Science ®Google Scholar
• Konstantinidis KV, Alici E, Aints A, Christensson B, Ljunggren H-G, Dilber MS. Targeting IL-2 to the endoplasmic reticulum confines autocrine growth stimulation to NK-92 cells. Exp Hematol. 2005;33:159–164. doi:10.1016/j.exphem.2004.11.003.
   PubMed Web of Science ®Google Scholar
• Sackmann EK, Fulton AL, Beebe DJ. The present and future role of microfluidics in biomedical research. Nature. 2014;507:181–189. doi:10.1038/nature13118.
   PubMed Web of Science ®Google Scholar
• Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol. 2014;32:760–772. doi:10.1038/nbt.2989.
   PubMed Web of Science ®Google Scholar
• Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science. 2010;328:1662–1668. doi:10.1126/science.1188302.
   PubMed Web of Science ®Google Scholar
• Jeon JS, Bersini S, Gilardi M, Dubini G, Charest JL, Moretti M, Kamm RD. Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation. Proc Natl Acad Sci USA. 2015;112:214–219. doi:10.1073/pnas.1417115112.
   PubMed Web of Science ®Google Scholar
• Jimenez-Torres JA, Peery SL, Sung KE, Beebe DJ. LumeNEXT: a practical method to pattern luminal structures in ECM gels. Adv Healthc Mater. 2016;5:198–204. doi:10.1002/adhm.201500608.
   PubMed Web of Science ®Google Scholar
• Sobrino A, Phan DTT, Datta R, Wang X,  Hachey SJ, Romero-López M, Gratton E, Lee AP, George SC, Hughes CCW. 3D microtumors in vitro supported by perfused vascular networks. Sci Rep-Uk. 2016;6.
   Web of Science ®Google Scholar
• Kurokawa YK, Yin RT, Shang MR, Shirure VS, Moya ML, George SC. Human induced pluripotent stem cell-derived endothelial cells for three-dimensional microphysiological systems. Tissue Eng Part C-Me. 2017;23:474–484. doi:10.1089/ten.tec.2017.0133.
   PubMed Web of Science ®Google Scholar
• Pavesi A, Tan AT, Koh S, Chia A, Colombo M, Antonecchia E, Miccolis C, Ceccarello E, Adriani G, Raimondi MT, et al. A 3D microfluidic model for preclinical evaluation of TCR-engineered T cells against solid tumors. Jci Insight. 2017;2.
   PubMed Web of Science ®Google Scholar
• Adriani G, Pavesi A, Tan AT, Bertoletti A, Thiery JP, Kamm RD. Microfluidic models for adoptive cell-mediated cancer immunotherapies. Drug Discov Today. 2016;21:1472–1478. doi:10.1016/j.drudis.2016.05.006.
   PubMed Web of Science ®Google Scholar
• Christakou AE, Ohlin M, Onfelt B, Wiklund M. Ultrasonic three-dimensional on-chip cell culture for dynamic studies of tumor immune surveillance by natural killer cells. Lab Chip. 2015;15:3222–3231. doi:10.1039/c5lc00436e.
   PubMed Web of Science ®Google Scholar
• Melero I, Rouzaut A, Motz GT, Coukos G. T-Cell and NK-Cell infiltration into solid tumors: a key limiting factor for efficacious cancer immunotherapy. Cancer Discov. 2014;4:522–526. doi:10.1158/2159-8290.CD-13-0985.
   PubMed Web of Science ®Google Scholar
• Hoogstad-van Evert JS, Cany J, van Den Brand D, Oudenampsen M, Brock R, Torensma R, Bekkers RL, Jansen JH, Massuger LF, Dolstra H. Umbilical cord blood CD34(+) progenitor-derived NK cells efficiently kill ovarian cancer spheroids and intraperitoneal tumors in NOD/SCID/IL2Rg(null) mice. Oncoimmunology. 2017;6:e1320630. doi:10.1080/2162402X.2017.1320630.
   PubMed Web of Science ®Google Scholar
• Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, Coussens LM, Gabrilovich DI, Ostrand-Rosenberg S, Hedrick CC, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24:541–550. doi:10.1038/s41591-018-0014-x.
   PubMed Web of Science ®Google Scholar
• Berthier E, Young EW, Beebe D. Engineers are from PDMS-land, biologists are from polystyrenia. Lab Chip. 2012;12:1224–1237. doi:10.1039/c2lc20982a.
   PubMed Web of Science ®Google Scholar
• Klingemann HG, Miyagawa B. Purging of malignant cells from blood after short ex vivo incubation with NK-92 cells. Blood. 1996;87:4913–4914.
   PubMed Web of Science ®Google Scholar
• Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994;8:652–658.
   PubMed Web of Science ®Google Scholar
• Tonn T, Schwabe D, Klingemann HG, Becker S, Esser R, Koehl U, Suttorp M, Seifried E, Ottmann OG, Bug G. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy. 2013;15:1563–1570. doi:10.1016/j.jcyt.2013.06.017.
   PubMed Web of Science ®Google Scholar
• Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J, Klingemann H. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy. 2008;10:625–632. doi:10.1080/14653240802301872.
   PubMed Web of Science ®Google Scholar
• Gillies SD. A new platform for constructing antibody-cytokine fusion proteins (immunocytokines) with improved biological properties and adaptable cytokine activity. Protein Eng Des Sel. 2013;26:561–569. doi:10.1093/protein/gzt045.
   PubMed Web of Science ®Google Scholar
• Larson LN, Johansson C, Lindholm L, Holmgren J. Mouse monoclonal-antibodies for experimental immunotherapy promotes killing of tumor-cells. Int J Cancer. 1988;42:877–882.
   PubMed Web of Science ®Google Scholar