G-CSF as a suitable alternative to GM-CSF to boost dinutuximab-mediated neutrophil cytotoxicity in neuroblastoma treatment Article Swipe
Paula Martínez-Sanz
,
Dieke J. van Rees
,
Lieke M. J. van Zogchel
,
Bart Klein
,
Panagiota Bouti
,
Hugo Olsman
,
Karin Schornagel
,
Ivana Kok
,
Ali Sunak
,
Kira Leeuwenburg
,
Ilse Timmerman
,
Miranda P. Dierselhuis
,
Waleed M. Kholosy
,
Jan J. Molenaar
,
Robin van Bruggen
,
Timo K. van den Berg
,
Taco W. Kuijpers
,
Hanke L. Matlung
,
Godelieve A.M. Tytgat
,
Katka Franke
·
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1136/jitc-2020-002259
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1136/jitc-2020-002259
Background Current immunotherapy for patients with high-risk neuroblastoma involves the therapeutic antibody dinutuximab that targets GD2, a ganglioside expressed on the majority of neuroblastoma tumors. Opsonized tumor cells are killed through antibody-dependent cellular cytotoxicity (ADCC), a process mediated by various immune cells, including neutrophils. The capacity of neutrophils to kill dinutuximab-opsonized tumor cells can be further enhanced by granulocyte-macrophage colony-stimulating factor (GM-CSF), which has been shown in the past to improve responses to anti-GD2 immunotherapy. However, access to GM-CSF (sargramostim) is limited outside of Northern America, creating a high clinical need for an alternative method to stimulate dinutuximab responsiveness in the treatment of neuroblastoma. In this in vitro study, we have investigated whether clinically well-established granulocyte colony-stimulating factor (G-CSF) can be a potentially suitable alternative for GM-CSF in the dinutuximab immunotherapy regimen of patients with neuroblastoma. Methods We compared the capacity of neutrophils stimulated either in vitro or in vivo with GM-CSF or G-CSF to kill dinutuximab-opsonized GD2-positive neuroblastoma cell lines and primary patient tumor material. Blocking experiments with antibodies inhibiting either respective Fc gamma receptors (FcγR) or neutrophil integrin CD11b/CD18 demonstrated the involvement of these receptors in the process of ADCC. Flow cytometry and live cell microscopy were used to quantify and visualize neutrophil-neuroblastoma interactions. Results We found that G-CSF was as potent as GM-CSF in enhancing the killing capacity of neutrophils towards neuroblastoma cells. This was observed with in vitro stimulated neutrophils, and with in vivo stimulated neutrophils from both patients with neuroblastoma and healthy donors. Enhanced killing due to GM-CSF or G-CSF stimulation was consistent regardless of dinutuximab concentration, tumor-to-neutrophil ratio and concentration of the stimulating cytokine. Both GM-CSF and G-CSF stimulated neutrophils required FcγRIIa and CD11b/CD18 integrin to perform ADCC, and this was accompanied by trogocytosis of tumor material by neutrophils and tumor cell death in both stimulation conditions. Conclusions Our preclinical data support the use of G-CSF as an alternative stimulating cytokine to GM-CSF in the treatment of high-risk neuroblastoma with dinutuximab, warranting further testing of G-CSF in a clinical setting.
Related Topics
Concepts
Antibody-dependent cell-mediated cytotoxicity
Neuroblastoma
Immunotherapy
Cancer research
Medicine
Antibody
Immunology
Immune system
Receptor
Cell culture
Biology
Internal medicine
Monoclonal antibody
Genetics
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1136/jitc-2020-002259
- https://jitc.bmj.com/content/jitc/9/5/e002259.full.pdf
- OA Status
- gold
- Cited By
- 35
- References
- 58
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W3164360732
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
-
https://openalex.org/W3164360732Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1136/jitc-2020-002259Digital Object Identifier
- Title
-
G-CSF as a suitable alternative to GM-CSF to boost dinutuximab-mediated neutrophil cytotoxicity in neuroblastoma treatmentWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2021Year of publication
- Publication date
-
2021-05-01Full publication date if available
- Authors
-
Paula Martínez-Sanz, Dieke J. van Rees, Lieke M. J. van Zogchel, Bart Klein, Panagiota Bouti, Hugo Olsman, Karin Schornagel, Ivana Kok, Ali Sunak, Kira Leeuwenburg, Ilse Timmerman, Miranda P. Dierselhuis, Waleed M. Kholosy, Jan J. Molenaar, Robin van Bruggen, Timo K. van den Berg, Taco W. Kuijpers, Hanke L. Matlung, Godelieve A.M. Tytgat, Katka FrankeList of authors in order
- Landing page
-
https://doi.org/10.1136/jitc-2020-002259Publisher landing page
- PDF URL
-
https://jitc.bmj.com/content/jitc/9/5/e002259.full.pdfDirect link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
-
https://jitc.bmj.com/content/jitc/9/5/e002259.full.pdfDirect OA link when available
- Concepts
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Antibody-dependent cell-mediated cytotoxicity, Neuroblastoma, Immunotherapy, Cancer research, Medicine, Antibody, Immunology, Immune system, Receptor, Cell culture, Biology, Internal medicine, Monoclonal antibody, GeneticsTop concepts (fields/topics) attached by OpenAlex
- Cited by
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35Total citation count in OpenAlex
- Citations by year (recent)
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2025: 2, 2024: 5, 2023: 9, 2022: 15, 2021: 4Per-year citation counts (last 5 years)
- References (count)
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58Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.antibody | 11 |
| abstract_inverted_index.capacity | 45, 140, 220 |
| abstract_inverted_index.cellular | 32 |
| abstract_inverted_index.clinical | 89, 334 |
| abstract_inverted_index.compared | 138 |
| abstract_inverted_index.creating | 86 |
| abstract_inverted_index.cytokine | 316 |
| abstract_inverted_index.enhanced | 56 |
| abstract_inverted_index.integrin | 179, 280 |
| abstract_inverted_index.involves | 8 |
| abstract_inverted_index.majority | 21 |
| abstract_inverted_index.material | 292 |
| abstract_inverted_index.mediated | 37 |
| abstract_inverted_index.observed | 228 |
| abstract_inverted_index.patients | 4, 133, 242 |
| abstract_inverted_index.quantify | 201 |
| abstract_inverted_index.required | 276 |
| abstract_inverted_index.setting. | 335 |
| abstract_inverted_index.suitable | 123 |
| abstract_inverted_index.(GM-CSF), | 61 |
| abstract_inverted_index.Opsonized | 25 |
| abstract_inverted_index.cytokine. | 269 |
| abstract_inverted_index.cytometry | 193 |
| abstract_inverted_index.enhancing | 217 |
| abstract_inverted_index.expressed | 18 |
| abstract_inverted_index.high-risk | 6, 323 |
| abstract_inverted_index.including | 42 |
| abstract_inverted_index.material. | 165 |
| abstract_inverted_index.receptors | 175, 186 |
| abstract_inverted_index.responses | 71 |
| abstract_inverted_index.stimulate | 96 |
| abstract_inverted_index.treatment | 101, 321 |
| abstract_inverted_index.visualize | 203 |
| abstract_inverted_index.Background | 0 |
| abstract_inverted_index.CD11b/CD18 | 180, 279 |
| abstract_inverted_index.antibodies | 169 |
| abstract_inverted_index.clinically | 113 |
| abstract_inverted_index.consistent | 257 |
| abstract_inverted_index.inhibiting | 170 |
| abstract_inverted_index.microscopy | 197 |
| abstract_inverted_index.neutrophil | 178 |
| abstract_inverted_index.regardless | 258 |
| abstract_inverted_index.respective | 172 |
| abstract_inverted_index.stimulated | 143, 232, 238, 274 |
| abstract_inverted_index.warranting | 327 |
| abstract_inverted_index.Conclusions | 303 |
| abstract_inverted_index.accompanied | 287 |
| abstract_inverted_index.alternative | 93, 124, 314 |
| abstract_inverted_index.conditions. | 302 |
| abstract_inverted_index.dinutuximab | 12, 97, 129, 260 |
| abstract_inverted_index.experiments | 167 |
| abstract_inverted_index.ganglioside | 17 |
| abstract_inverted_index.granulocyte | 115 |
| abstract_inverted_index.involvement | 183 |
| abstract_inverted_index.neutrophils | 47, 142, 222, 239, 275, 294 |
| abstract_inverted_index.potentially | 122 |
| abstract_inverted_index.preclinical | 305 |
| abstract_inverted_index.stimulating | 268, 315 |
| abstract_inverted_index.stimulation | 255, 301 |
| abstract_inverted_index.therapeutic | 10 |
| abstract_inverted_index.GD2-positive | 157 |
| abstract_inverted_index.cytotoxicity | 33 |
| abstract_inverted_index.demonstrated | 181 |
| abstract_inverted_index.dinutuximab, | 326 |
| abstract_inverted_index.investigated | 111 |
| abstract_inverted_index.neutrophils, | 233 |
| abstract_inverted_index.neutrophils. | 43 |
| abstract_inverted_index.trogocytosis | 289 |
| abstract_inverted_index.concentration | 265 |
| abstract_inverted_index.immunotherapy | 2, 130 |
| abstract_inverted_index.interactions. | 205 |
| abstract_inverted_index.neuroblastoma | 7, 23, 158, 224, 244, 324 |
| abstract_inverted_index.(sargramostim) | 79 |
| abstract_inverted_index.concentration, | 261 |
| abstract_inverted_index.immunotherapy. | 74 |
| abstract_inverted_index.neuroblastoma. | 103, 135 |
| abstract_inverted_index.responsiveness | 98 |
| abstract_inverted_index.well-established | 114 |
| abstract_inverted_index.antibody-dependent | 31 |
| abstract_inverted_index.colony-stimulating | 59, 116 |
| abstract_inverted_index.tumor-to-neutrophil | 262 |
| abstract_inverted_index.dinutuximab-opsonized | 50, 156 |
| abstract_inverted_index.granulocyte-macrophage | 58 |
| abstract_inverted_index.neutrophil-neuroblastoma | 204 |
| cited_by_percentile_year.max | 99 |
| cited_by_percentile_year.min | 95 |
| corresponding_author_ids | https://openalex.org/A5052030168 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 20 |
| corresponding_institution_ids | https://openalex.org/I3020210244 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/3 |
| sustainable_development_goals[0].score | 0.75 |
| sustainable_development_goals[0].display_name | Good health and well-being |
| citation_normalized_percentile.value | 0.94849085 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | True |