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OncoImmunology Volume 7, 2018 - Issue 4
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Original Research

Activated human primary NK cells efficiently kill colorectal cancer cells in 3D spheroid cultures irrespectively of the level of PD-L1 expression

Pilar M. LanuzaAragón Health Research Institute (IIS Aragón), Zaragoza, SpainView further author information
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Alan ViguerasAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Group of Applied Mechanics and Bioengineering (AMB); Instituto de Investigación en Ingeniería de Aragón (I3A), Universidad de Zaragoza, Spain;Centro Investigacion Biomedica en Red. Bioingenieria, biomateriales y nanomedicina (CIBER-BBN)View further author information
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Sara OlivanAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Group of Applied Mechanics and Bioengineering (AMB); Instituto de Investigación en Ingeniería de Aragón (I3A), Universidad de Zaragoza, Spain;Centro Investigacion Biomedica en Red. Bioingenieria, biomateriales y nanomedicina (CIBER-BBN)View further author information
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Anne C. PratsInserm, U1037, F-31432 Toulouse, France, Université de Toulouse, UPS, Cancer Research Center of Toulouse, F-31432 Toulouse, FranceView further author information
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Santiago CostasAragón Health Research Institute (IIS Aragón), Zaragoza, SpainView further author information
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Guillermo LlamazaresAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Group of Applied Mechanics and Bioengineering (AMB); Instituto de Investigación en Ingeniería de Aragón (I3A), Universidad de Zaragoza, Spain;Centro Investigacion Biomedica en Red. Bioingenieria, biomateriales y nanomedicina (CIBER-BBN)View further author information
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Diego Sanchez-MartinezAragón Health Research Institute (IIS Aragón), Zaragoza, SpainView further author information
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José María AyusoMedical Engineering, Morgridge Institute for Research, Madison, Wisconsin, USA;Department of Biomedical Engineering, Wisconsin Institutes for Medical Research, University of Wisconsin, Madison, WI, USA;The University of Wisconsin Carbone Cancer Center, University of Wisconsin, Madison, WI, USAView further author information
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Luis FernandezAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Group of Applied Mechanics and Bioengineering (AMB); Instituto de Investigación en Ingeniería de Aragón (I3A), Universidad de Zaragoza, Spain;Centro Investigacion Biomedica en Red. Bioingenieria, biomateriales y nanomedicina (CIBER-BBN)View further author information
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Ignacio OchoaAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Group of Applied Mechanics and Bioengineering (AMB); Instituto de Investigación en Ingeniería de Aragón (I3A), Universidad de Zaragoza, Spain;Centro Investigacion Biomedica en Red. Bioingenieria, biomateriales y nanomedicina (CIBER-BBN)Correspondence[email protected]
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&
Julián PardoAragón Health Research Institute (IIS Aragón), Zaragoza, Spain;Dpt. Microbiology, Preventive Medicine and Public Health and Dpt. Biochemistry and Molecular and Cell Biology, University of Zaragoza, Zaragoza, Spain;Aragón I+D Foundation (ARAID), Government of Aragon, Zaragoza, Spain Nanoscience Institute of Aragon (INA), University of Zaragoza, Zaragoza, SpainCorrespondence[email protected]
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Article: e1395123 | Received 02 Jun 2017, Accepted 16 Oct 2017, Published online: 12 Feb 2018

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Cecilia Pesini, Sandra Hidalgo, Maykel A. Arias, Llipsy Santiago, Carlota Calvo, Maitane Ocariz-Díez, Dolores Isla, Pilar M. Lanuza, M José Agustín, Eva M Galvez, Ariel Ramírez-Labrada & Julián Pardo. (2022) PD-1 is expressed in cytotoxic granules of NK cells and rapidly mobilized to the cell membrane following recognition of tumor cells. OncoImmunology 11:1.
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Chantal Reina-Ortiz, Michael Constantinides, Alexis Fayd-Herbe-de-Maudave, Jessy Présumey, Javier Hernandez, Guillaume Cartron, David Giraldos, Rosana Díez, Isabel Izquierdo, Gemma Azaceta, Luis Palomera, Isabel Marzo, Javier Naval, Alberto Anel & Martín Villalba. (2021) Expanded NK cells from umbilical cord blood and adult peripheral blood combined with daratumumab are effective against tumor cells from multiple myeloma patients. OncoImmunology 10:1.
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Articles from other publishers (28)

Ivana Kutle, Robert Polten, Jens Hachenberg, Rüdiger Klapdor, Michael Morgan & Axel Schambach. (2023) Tumor Organoid and Spheroid Models for Cervical Cancer. Cancers 15:9, pages 2518.
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Farhoodeh Ghaedrahmati, Nafiseh Esmaeil & Maryam Abbaspour. (2022) Targeting immune checkpoints: how to use natural killer cells for fighting against solid tumors. Cancer Communications 43:2, pages 177-213.
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Meng-Wei Ko, Kawaljit Kaur, Po-Chun Chen, Barbara Breznik, Emanuela Senjor, Nishant Chovatiya, Paul Wong, Tamara Lah Turnsek, Janko Kos & Anahid Jewett. 2023. NK Cells in Cancer Immunotherapy: Successes and Challenges. NK Cells in Cancer Immunotherapy: Successes and Challenges 281 297 .
Pilar M. Lanuza, M. Henar Alonso, Sandra Hidalgo, Iratxe Uranga-Murillo, Sandra García-Mulero, Raquel Arnau, Cristina Santos, Xavier Sanjuan, Llipsy Santiago, Laura Comas, Sergio Redrado, Roberto Pazo-Cid, M. Jose Agustin-Ferrández, Paula Jaime-Sánchez, Cecilia Pesini, Eva M. Gálvez, Ariel Ramírez-Labrada, Maykel Arias, Rebeca Sanz-Pamplona & Julián Pardo. (2022) Adoptive NK Cell Transfer as a Treatment in Colorectal Cancer Patients: Analyses of Tumour Cell Determinants Correlating With Efficacy In Vitro and In Vivo. Frontiers in Immunology 13.
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Veronica Huber, Viviana Vallacchi, Elena Daveri & Elisabetta Vergani. (2022) 3D models for melanoma γδ T cell‐based immunotherapy. Clinical and Translational Medicine 12:6.
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Lingling Ou, Huaishan Wang, Hui Huang, Zhiyan Zhou, Qiang Lin, Yeye Guo, Tara Mitchell, Alexander C. Huang, Giorgos Karakousis, Lynn Schuchter, Ravi Amaravadi, Wei Guo, Joseph Salvino, Meenhard Herlyn & Xiaowei Xu. (2022) Preclinical platforms to study therapeutic efficacy of human γδ T cells. Clinical and Translational Medicine 12:6.
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Pankaj Ahluwalia, Ashis K. Mondal, Meenakshi Ahluwalia, Nikhil S. Sahajpal, Kimya Jones, Yasmeen Jilani, Gagandeep K. Gahlay, Amanda Barrett, Vamsi Kota, Amyn M. Rojiani & Ravindra Kolhe. (2022) Clinical and molecular assessment of an onco‐immune signature with prognostic significance in patients with colorectal cancer . Cancer Medicine 11:6, pages 1573-1586.
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Elaheh Dalir Abdolahinia, Ghasem Barati, Zahra Ranjbar-Navazi, Jamileh Kadkhoda, Maryam Islami, Nastaran Hashemzadeh, Solmaz Maleki Dizaj & Simin Sharifi. (2022) Application of nanogels as drug delivery systems in multicellular spheroid tumor model. Journal of Drug Delivery Science and Technology 68, pages 103109.
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Fengyun Zhong, Yilin Lin, Xiangxiang Jing, Yingjiang Ye, Shan Wang & Zhanlong Shen. (2022) Innate tumor killers in colorectal cancer. Cancer Letters 527, pages 115-126.
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Oanh T. P. Nguyen, Patrick M. Misun, Christian Lohasz, Jihyun Lee, Weijia Wang, Timm Schroeder & Andreas Hierlemann. (2021) An Immunocompetent Microphysiological System to Simultaneously Investigate Effects of Anti-Tumor Natural Killer Cells on Tumor and Cardiac Microtissues. Frontiers in Immunology 12.
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Angélica Díaz‐Basabe, Claudia Burrello, Georgia Lattanzi, Fiorenzo Botti, Alberto Carrara, Elisa Cassinotti, Flavio Caprioli & Federica Facciotti. (2021) Human intestinal and circulating invariant natural killer T cells are cytotoxic against colorectal cancer cells via the perforin–granzyme pathway. Molecular Oncology 15:12, pages 3385-3403.
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J. Singh, S. Hatcher, A.A. Ku, Z. Ding, F.Y. Feng, R.A. Sharma & S.X. Pfister. (2021) Model Selection for the Preclinical Development of New Drug–Radiotherapy Combinations. Clinical Oncology 33:11, pages 694-704.
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Yuta Ando, Chelsea Mariano & Keyue Shen. (2021) Engineered in vitro tumor models for cell-based immunotherapy. Acta Biomaterialia 132, pages 345-359.
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Alessandro Poggi, Federico Villa, Jordi Leonardo Castrillo Fernadez, Delfina Costa, Maria Raffaella Zocchi & Roberto Benelli. (2021) Three-Dimensional Culture Models to Study Innate Anti-Tumor Immune Response: Advantages and Disadvantages. Cancers 13:14, pages 3417.
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Nayoung Kim, Dong-Hee Lee, Woo Seon Choi, Eunbi Yi, HyoJeong Kim, Jung Min Kim, Hyung-Seung Jin & Hun Sik Kim. (2021) Harnessing NK cells for cancer immunotherapy: immune checkpoint receptors and chimeric antigen receptors. BMB Reports 54:1, pages 44-58.
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Honglin Shen, Shuxiang Cai, Chuanxiang Wu, Wenguang Yang, Haibo Yu & Lianqing Liu. (2021) Recent Advances in Three-Dimensional Multicellular Spheroid Culture and Future Development. Micromachines 12:1, pages 96.
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Yuqing Cao, Xiaoyu Wang, Tianqiang Jin, Yu Tian, Chaoliu Dai, Crystal Widarma, Rui Song & Feng Xu. (2020) Immune checkpoint molecules in natural killer cells as potential targets for cancer immunotherapy. Signal Transduction and Targeted Therapy 5:1.
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Madison N. Temples, Isaac M. Adjei, Phoebe M. Nimocks, Julie Djeu & Blanka Sharma. (2020) Engineered Three-Dimensional Tumor Models to Study Natural Killer Cell Suppression. ACS Biomaterials Science & Engineering 6:7, pages 4179-4199.
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Muhammad Khan, Sumbal Arooj & Hua Wang. (2020) NK Cell-Based Immune Checkpoint Inhibition. Frontiers in Immunology 11.
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Pilar M. Lanuza, Cecilia Pesini, Maykel A. Arias, Carlota Calvo, Ariel Ramirez-Labrada & Julian Pardo. (2020) Recalling the Biological Significance of Immune Checkpoints on NK Cells: A Chance to Overcome LAG3, PD1, and CTLA4 Inhibitory Pathways by Adoptive NK Cell Transfer?. Frontiers in Immunology 10.
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J. K. H. Leman, L. Munoz-Erazo & R. A. Kemp. 2020. Tumor Microenvironments in Organs. Tumor Microenvironments in Organs 1 22 .
Tristan Courau, Julie Bonnereau, Justine Chicoteau, Hugo Bottois, Romain Remark, Laura Assante Miranda, Antoine Toubert, Mathieu Blery, Thomas Aparicio, Matthieu Allez & Lionel Le Bourhis. (2019) Cocultures of human colorectal tumor spheroids with immune cells reveal the therapeutic potential of MICA/B and NKG2A targeting for cancer treatment. Journal for ImmunoTherapy of Cancer 7:1.
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Jose M. Ayuso, Ross Vitek, Adam D. Swick, Melissa C. Skala, Kari B. Wisinski, Randall J. Kimple, Paul F. Lambert & David J. Beebe. (2019) Effects of culture method on response to EGFR therapy in head and neck squamous cell carcinoma cells. Scientific Reports 9:1.
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Nayoung Kim, Hyeon Ho Lee, Hyo-Jung Lee, Woo Seon Choi, Jinju Lee & Hun Sik Kim. (2019) Natural killer cells as a promising therapeutic target for cancer immunotherapy. Archives of Pharmacal Research 42:7, pages 591-606.
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Noha Mousaad Elemam, Zaidoon Al-Jaderi, Mahmood Yaseen Hachim & Azzam A. Maghazachi. (2019) HCT-116 colorectal cancer cells secrete chemokines which induce chemoattraction and intracellular calcium mobilization in NK92 cells. Cancer Immunology, Immunotherapy 68:6, pages 883-895.
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Barbara Bassani, Denisa Baci, Matteo Gallazzi, Alessandro Poggi, Antonino Bruno & Lorenzo Mortara. (2019) Natural Killer Cells as Key Players of Tumor Progression and Angiogenesis: Old and Novel Tools to Divert Their Pro-Tumor Activities into Potent Anti-Tumor Effects. Cancers 11:4, pages 461.
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Keisuke Teshigawara, Sho Nagai, Gaowa Bai, Yuji Okubo, Haorile Chagan-Yasutan & Toshio Hattori. (2018) Successful Amplified-Natural-Killer Cell (ANK) Therapy Administered to a Patient with Smoldering Adult T-Cell Leukemia in Acute Crisis. Reports 1:2, pages 13.
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