Nanowire Based Guidance of the Morphology and Cytotoxic Activity of Natural Killer Cells.

biofunctionalization immunotherapy natural killer cells silicon nanowires site selective functionalization

Journal

Small (Weinheim an der Bergstrasse, Germany)
ISSN: 1613-6829
Titre abrégé: Small
Pays: Germany
ID NLM: 101235338

Informations de publication

Date de publication:
04 2021
Historique:
revised: 13 01 2021
received: 22 11 2020
pubmed: 16 3 2021
medline: 15 7 2021
entrez: 15 3 2021
Statut: ppublish

Résumé

The cytotoxic activity of natural killer (NK) cells is regulated by many chemical and physical cues, whose integration mechanism is still obscure. Here, a multifunctional platform is engineered for NK cell stimulation, to study the effect of the signal integration and spatial heterogeneity on NK cell function. The platform is based on nanowires, whose mechanical compliance and site-selective tip functionalization with antigens produce the physical and chemical stimuli, respectively. The nanowires are confined to micron-sized islands, which induce a splitting of the NK cells into two subpopulations with distinct morphologies and immune responses: NK cells atop the nanowire islands display symmetrical spreading and enhanced activation, whereas cells lying in the straits between the islands develop elongated profiles and show lower activation levels. The demonstrated tunability of NK cell cytotoxicity provides an important insight into the mechanism of their immune function and introduces a novel technological route for the ex vivo shaping of cytotoxic lymphocytes in immunotherapy.

Identifiants

pubmed: 33719212
doi: 10.1002/smll.202007347
doi:

Substances chimiques

Antigens 0
Antineoplastic Agents 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2007347

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

The Immune Synapse, Methods and Protocols (Eds: C. T. Baldari, M. L. Dustin), Humana Press, Totowa, NJ 2017.
S. K. Bromley, W. R. Burack, K. G. Johnson, K. Somersalo, T. N. Sims, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, M. L. Dustin, Annu. Rev. Immunol. 2001, 19, 375.
A. Grakoui, S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, M. L. Dustin, Science 1999, 285, 221.
M. J. P. Biggs, M. C. Milone, L. C. Santos, A. Gondarenko, S. J. Wind, J. R. Soc., Interface 2011, 8, 1462.
J. H. Jang, Y. Huang, P. Zheng, M. C. Jo, G. Bertolet, M. X. Zhu, L. Qin, D. Liu, J. Immunol. 2015, 195, 1320.
S. V. Pageon, T. Tabarin, Y. Yamamoto, Y. Ma, J. S. Bridgeman, A. Cohnen, C. Benzing, Y. Gao, M. D. Crowther, K. Tungatt, G. Dolton, A. K. Sewell, D. A. Price, O. Acuto, R. G. Parton, J. J. Gooding, J. Rossy, J. Rossjohn, K. Gaus, Proc. Natl. Acad. Sci. USA 2016, 113, E5454.
M. F. Krummel, M. M. Davis, Curr. Opin. Immunol. 2002, 14, 66.
M. L. Dustin, J. T. Groves, Annu. Rev. Biophys. 2012, 41, 543.
B. F. Lillemeier, M. A. Mörtelmaier, M. B. Forstner, J. B. Huppa, J. T. Groves, M. M. Davis, Nat. Immunol. 2010, 11, 90.
Y. Jung, I. Riven, S. W. Feigelson, E. Kartvelishvily, K. Tohya, M. Miyasaka, R. Alon, G. Haran, Proc. Natl. Acad. Sci. USA 2016, 113, E5916.
R. Basu, M. Huse, Trends Cell Biol. 2017, 27, 241.
J. A. Hammer, J. K. Burkhardt, Curr. Opin. Immunol. 2013, 25, 300.
A. Le Floc'h, M. Huse, Cell. Mol. Life Sci. 2015, 72, 537.
E. Natkanski, W. Y. Lee, B. Mistry, A. Casal, J. E. Molloy, P. Tolar, Science 2013, 340, 1587.
E. Judokusumo, E. Tabdanov, S. Kumari, M. L. Dustin, L. C. Kam, Biophys. J. 2012, 102, L5.
H. H. Lin, H. K. Lin, I. H. Lin, Y. W. Chiou, H. W. Chen, C. Y. Liu, H. I. C. Harn, W. T. Chiu, Y. K. Wang, M. R. Shen, M.-J. Tang, Oncotarget 2015, 6, 20946.
D. Wirtz, K. Konstantopoulos, P. C. Searson, Nat. Rev. Cancer 2011, 11, 512.
L. K. Chin, Y. Xia, D. E. Discher, P. A. Janmey, Curr. Opin. Chem. Eng. 2016, 11, 77.
N. Bufi, M. Saitakis, S. Dogniaux, O. Buschinger, A. Bohineust, A. Richert, M. Maurin, C. Hivroz, A. Asnacios, Biophys. J. 2015, 108, 2181.
G. Le Saux, M. Schvartzman, Int. J. Mol. Sci. 2019, 20, 646.
F. J. Culley, M. Johnson, J. H. Evans, S. Kumar, R. Crilly, J. Casasbuenas, T. Schnyder, M. Mehrabi, M. P. Deonarain, D. S. Ushakov, V. Braud, G. Roth, R. Brock, K. Köhler, D. M. Davis, PLoS Biol. 2009, 7, e1000159.
G. Le Saux, N. Bar-Hanin, A. Edri, U. Hadad, A. Porgador, M. Schvartzman, Adv. Mater. 2019, 31, 1805954.
G. Ferlazzo, M. L. Tsang, L. Moretta, G. Melioli, R. M. Steinman, C. Münz, J. Exp. Med. 2002, 195, 343.
Y. Keydar, G. Le Saux, A. Pandey, E. Avishay, N. Bar-Hanin, T. Esti, V. Bhingardive, U. Hadad, A. Porgador, M. Schvartzman, Nanoscale 2018, 10, 14651.
L. Mordechay, G. Le Saux, A. Edri, U. Hadad, A. Porgador, M. Schvartzman, ACS Biomater. Sci. Eng. 2020, 7, 122.
D. Blumenthal, V. Chandra, L. Avery, J. K. Burkhardt, eLife 2020, 9, e55995.
W. Park, G. Zheng, X. Jiang, B. Tian, C. M. Lieber, Nano Lett. 2008, 8, 3004.
P. Xie, Y. Hu, Y. Fang, J. Huang, C. M. Lieber, Proc. Natl. Acad. Sci. USA 2009, 106, 15254
Y. Cui, L. J. Lauhon, M. S. Gudiksen, J. Wang, C. M. Lieber, Appl. Phys. Lett. 2001, 78, 2214.
M. H. Huang, Y. Wu, H. Feick, N. Tran, E. Weber, P. Yang, Adv. Mater. 2001, 13, 113.
Y. Wu, Y. Cui, L. Huynh, C. J. Barrelet, D. C. Bell, C. M. Lieber, Nano Lett. 2004, 4, 433.
A. B. Greytak, L. J. Lauhon, M. S. Gudiksen, C. M. Lieber, Appl. Phys. Lett. 2004, 84, 4176.
Z. Jiang, Q. Qing, P. Xie, R. Gao, C. M. Lieber, Nano Lett. 2012, 12, 1711.
B. Tian, P. Xie, T. J. Kempa, D. C. Bell, C. M. Lieber, Nat. Nanotechnol. 2009, 4, 824.
L. Xu, Z. Jiang, Q. Qing, L. Mai, Q. Zhang, C. M. Lieber, Nano Lett. 2013, 13, 746.
W. Hallstrom, M. Lexholm, D. B. Suyatin, G. Hammarin, D. Hessman, L. Samuelson, L. Montelius, M. Kanje, C. N. Prinz, Nano Lett. 2010, 10, 782.
P. K. Sahoo, R. Janissen, M. P. Monteiro, A. Cavalli, D. M. Murillo, M. V Merfa, C. L. Cesar, H. F. Carvalho, A. A. De Souza, E. P. A. M. Bakkers, M. A. Cotta, Nano Lett. 2016, 16, 4656.
A. K. Shalek, J. T. Gaublomme, L. Wang, N. Yosef, N. Chevrier, M. S. Andersen, J. T. Robinson, N. Pochet, D. Neuberg, R. S. Gertner, I. Amit, J. R. Brown, N. Hacohen, A. Regev, C. J. Wu, H. Park, Nano Lett. 2012, 12, 6498.
Y. R. Na, S. Y. Kim, J. T. Gaublomme, A. K. Shalek, M. Jorgolli, H. Park, E. G. Yang, Nano Lett. 2013, 13, 153.
N. Yosef, A. K. Shalek, J. T. Gaublomme, H. Jin, Y. Lee, A. Awasthi, C. Wu, K. Karwacz, S. Xiao, M. Jorgolli, D. Gennert, R. Satija, A. Shakya, D. Y. Lu, J. J. Trombetta, M. R. Pillai, P. J. Ratcliffe, M. L. Coleman, M. Bix, D. Tantin, H. Park, V. K. Kuchroo, A. Regev, Nature 2013, 496, 461.
C. N. Prinz, J. Phys.: Condens. Matter 2015, 27, 233103.
L. Hanson, Z. C. Lin, C. Xie, Y. Cui, B. Cui, Nano Lett. 2012, 12, 5815.
T. Berthing, S. Bonde, K. R. Rostgaard, M. H. Madsen, C. B. Sorensen, J. Nygård, K. L. Martinez, Nanotechnology 2012, 23, 415102.
M. A. Cooper, T. A. Fehniger, M. A. Caligiuri, Trends Immunol. 2001, 22, 633.
J. K. Burkhardt, S. Hester, Y. Argon, Proc. Natl. Acad. Sci. USA 1989, 86, 7128.
A. Moretta, C. Bottino, M. C. Mingari, R. Biassoni, L. Moretta, Nat. Immunol. 2002, 3, 6.
N. J. Topham, E. W. Hewitt, Immunology 2009, 128, 7.
J. S. Orange, Nat. Rev. Immunol. 2008, 8, 713.
M. Fukuda, J. Biol. Chem. 1991, 266, 21327.
E. Aktas, U. C. Kucuksezer, S. Bilgic, G. Erten, G. Deniz, Cell. Immunol. 2009, 254, 149.
G. Alter, J. M. Malenfant, M. Altfeld, J. Immunol. Methods 2004, 294, 15.
A. Y. Mah, M. A. Cooper, Crit. Rev. Immunol. 2016, 36, 131.
P. Bhat, G. Leggatt, N. Waterhouse, I. H. Frazer, Cell Death Dis. 2017, 8, e2836.
D. Delcassian, D. Depoil, D. Rudnicka, M. Liu, D. M. Davis, M. L. Dustin, I. E. Dunlop, Nano Lett. 2013, 13, 5608.
W. Abuillan, Fine-Structures, Lateral Correlation and Diffusion of Membrane-Associated Proteins on Biological Membrane Surfaces. Diss. 2013.
L. J. Harris, E. Skaletsky, A. McPherson, J. Mol. Biol. 1998, 275, 861.
L. D. Landau, E. M. Lifshits⁀, A. M. Kosevich, L. P. Pitaevskiĭ, Theory of Elasticity, Butterworth-Heinemann, Oxford, UK 1986.
S. T. Kim, Y. Shin, K. Brazin, R. J. Mallis, Z.-Y. J. Sun, G. Wagner, M. J. Lang, E. L. Reinherz, Front. Immunol. 2012, 3, 76.
J. Hong, C. Ge, P. Jothikumar, Z. Yuan, B. Liu, K. Bai, K. Li, W. Rittase, M. Shinzawa, Y. Zhang, A. Palin, P. Love, X. Yu, K. Salaita, B. D. Evavold, A. Singer, C. Zhu, Nat. Immunol. 2018, 19, 1379.
Y. Zeng, J. Yi, Z. Wan, K. Liu, P. Song, A. Chau, F. Wang, Z. Chang, W. Han, W. Zheng, Y. H. Chen, C. Xiong, W. Liu, Eur. J. Immunol. 2015, 45, 1621.
Z. Wan, S. Zhang, Y. Fan, K. Liu, A. M. Davey, H. Zhang, W. Han, C. Xiong, W. Liu, J. Immunol. 2013, 190, 4661.
M. Saitakis, S. Dogniaux, C. Goudot, N. Bufi, S. Asnacios, M. Maurin, C. Randriamampita, A. Asnacios, C. Hivroz, eLife 2017, 6, e23190.
R. S. O'Connor, X. Hao, K. Shen, K. Bashour, T. Akimova, W. W. Hancock, L. C. Kam, M. C. Milone, J. Immunol. 2012, 189, 1330.
O. Matalon, A. Ben-Shmuel, J. Kivelevitz, B. Sabag, S. Fried, N. Joseph, E. Noy, G. Biber, M. Barda-Saad, EMBO J. 2018, 37, 96264.
B. Vanherberghen, P. E. Olofsson, E. Forslund, M. Sternberg-Simon, M. A. Khorshidi, S. Pacouret, K. Guldevall, M. Enqvist, K.-J. Malmberg, R. Mehr, B. Önfelt, Blood 2013, 121, 1326.
K. Guldevall, L. Brandt, E. Forslund, K. Olofsson, T. W. Frisk, P. E. Olofsson, K. Gustafsson, O. Manneberg, B. Vanherberghen, H. Brismar, K. Kärre, M. Uhlin, B. Önfelt, Front. Immunol. 2016, 7, 119.
P. Verdijk, P. A. van Veelen, A. H. de Ru, P. J. Hensbergen, K. Mizuno, H. K. Koerten, F. Koning, C. P. Tensen, A. M. Mommaas, Eur. J. Immunol. 2004, 34, 156.
S. A. Rosenberg, N. P. Restifo, Science 2015, 348, 62.
C. H. June, S. R. Riddell, T. N. Schumacher, Sci. Transl. Med. 2015, 7, 280ps7.
R. J. Brentjens, I. Rivière, J. H. Park, M. L. Davila, X. Wang, J. Stefanski, C. Taylor, R. Yeh, S. Bartido, O. Borquez-Ojeda, M. Olszewska, Y. Bernal, H. Pegram, M. Przybylowski, D. Hollyman, Y. Usachenko, D. Pirraglia, J. Hosey, E. Santos, E. Halton, P. Maslak, D. Scheinberg, J. Jurcic, M. Heaney, G. Heller, M. Frattini, M. Sadelain, Blood 2011, 118, 4817.
S. S. Neelapu, F. L. Locke, N. L. Bartlett, L. Lekakis, D. Miklos, C. A. Jacobson, I. Braunschweig, O. Oluwole, T. Siddiqi, Y. Lin, J. Timmerman, P. J. Stiff, J. Friedberg, I. Flinn, A. Goy, M. Smith, A. Deol, U. Farooq, P. McSweeney, J. Munoz, I. Avivi, J. E. Castro, J. R. Westin, J. C. Chavez, A. Ghobadi, K. V. Komanduri, R. Levy, E. D. Jacobsen, P. Reagan, A. Bot, J. M. Rossi, L. Navale, Y. Jiang, J. S. Aycock, M. Elias, J. Wiezorek, W. Y. Go, Blood 2016, 128, 998.
A. P. Dang, S. De Leo, D. R. Bogdanowicz, D. J. Yuan, S. M. Fernandes, J. R. Brown, H. H. Lu, L. C. Kam, Adv. Biosyst. 2018, 2, 1700167.
L. H. Lambert, G. K. E. Goebrecht, S. E. De Leo, R. S. O'Connor, S. Nunez-Cruz, T. De Li, J. Yuan, M. C. Milone, L. C. Kam, Nano Lett. 2017, 17, 821.

Auteurs

Viraj Bhingardive (V)

Department of Materials Engineering, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.
Ilse Katz Institute for Nanoscale Science and Technology, The Shraga Segal Department of Microbiology, Immunology, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.

Guillaume Le Saux (G)

Department of Materials Engineering, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.
Ilse Katz Institute for Nanoscale Science and Technology, The Shraga Segal Department of Microbiology, Immunology, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.

Avishay Edri (A)

Genetics Faculty of Health Sciences, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.

Angel Porgador (A)

Genetics Faculty of Health Sciences, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.

Mark Schvartzman (M)

Department of Materials Engineering, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.
Ilse Katz Institute for Nanoscale Science and Technology, The Shraga Segal Department of Microbiology, Immunology, Ben-Gurion University of the Negev, P.O. Box 653, Beer-Sheva, 84105, Israel.

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