A Multispectral 3D Live Organoid Imaging Platform to Screen Probes for Fluorescence Guided Surgery

Overview

Journal EMBO Mol Med

Specialty Molecular Biology

Date 2024 Jun 3

PMID 38831131

Authors

Bernadette Jeremiasse

Ravian L van Ineveld

Veerle Bok

Michiel Kleinnijenhuis

Sam de Blank

Maria Alieva

Hannah R Johnson

Esmee J van Vliet

Amber L Zeeman

Lianne M Wellens

Gerard Llibre-Palomar

Mario Barrera Roman

Alessia Di Maggio

Johanna F Dekkers

Sabrina Oliveira

Alexander L Vahrmeijer

Jan J Molenaar

Marc Hwa Wijnen

Alida Fw van der Steeg

Ellen J Wehrens

Anne C Rios

Affiliations

Soon will be listed here.

Abstract

Achieving complete tumor resection is challenging and can be improved by real-time fluorescence-guided surgery with molecular-targeted probes. However, pre-clinical identification and validation of probes presents a lengthy process that is traditionally performed in animal models and further hampered by inter- and intra-tumoral heterogeneity in target expression. To screen multiple probes at patient scale, we developed a multispectral real-time 3D imaging platform that implements organoid technology to effectively model patient tumor heterogeneity and, importantly, healthy human tissue binding.

Citing Articles

From Cancer to Immune Organoids: Innovative Preclinical Models to Dissect the Crosstalk between Cancer Cells and the Tumor Microenvironment.

Picca F, Giannotta C, Tao J, Giordanengo L, Munir H, Botta V Int J Mol Sci. 2024; 25(19).

PMID: 39409152 PMC: 11476904. DOI: 10.3390/ijms251910823.

References

Bergmann S, Lawler S, Qu Y, Fadzen C, Wolfe J, Regan M . Blood-brain-barrier organoids for investigating the permeability of CNS therapeutics. Nat Protoc. 2018; 13(12):2827-2843. PMC: 6673652. DOI: 10.1038/s41596-018-0066-x. View

Boogerd L, Boonstra M, Prevoo H, Handgraaf H, Kuppen P, van de Velde C . Fluorescence-guided tumor detection with a novel anti-EpCAM targeted antibody fragment: Preclinical validation. Surg Oncol. 2019; 28:1-8. DOI: 10.1016/j.suronc.2018.10.004. View

Burstein M, Tsimelzon A, Poage G, Covington K, Contreras A, Fuqua S . Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res. 2014; 21(7):1688-98. PMC: 4362882. DOI: 10.1158/1078-0432.CCR-14-0432. View

Calandrini C, Schutgens F, Oka R, Margaritis T, Candelli T, Mathijsen L . An organoid biobank for childhood kidney cancers that captures disease and tissue heterogeneity. Nat Commun. 2020; 11(1):1310. PMC: 7066173. DOI: 10.1038/s41467-020-15155-6. View

Dadario N, Khatri D, Reichman N, Nwagwu C, DAmico R . 5-Aminolevulinic Acid-Shedding Light on Where to Focus. World Neurosurg. 2021; 150:9-16. DOI: 10.1016/j.wneu.2021.02.118. View

Deken M, Bos D, Tummers W, March T, van de Velde C, Rijpkema M . Multimodal image-guided surgery of HER2-positive breast cancer using [In]In-DTPA-trastuzumab-IRDye800CW in an orthotopic breast tumor model. EJNMMI Res. 2019; 9(1):98. PMC: 6872692. DOI: 10.1186/s13550-019-0564-z. View

Deken M, Kijanka M, Hernandez I, Slooter M, de Bruijn H, van Diest P . Nanobody-targeted photodynamic therapy induces significant tumor regression of trastuzumab-resistant HER2-positive breast cancer, after a single treatment session. J Control Release. 2020; 323:269-281. PMC: 7116241. DOI: 10.1016/j.jconrel.2020.04.030. View

Dekkers J, van Vliet E, Sachs N, Rosenbluth J, Kopper O, Rebel H . Long-term culture, genetic manipulation and xenotransplantation of human normal and breast cancer organoids. Nat Protoc. 2021; 16(4):1936-1965. PMC: 8221035. DOI: 10.1038/s41596-020-00474-1. View

Doberstein K, Milde-Langosch K, Bretz N, Schirmer U, Harari A, Witzel I . L1CAM is expressed in triple-negative breast cancers and is inversely correlated with androgen receptor. BMC Cancer. 2014; 14:958. PMC: 4301892. DOI: 10.1186/1471-2407-14-958. View

10.

Galema H, Meijer R, Lauwerends L, Verhoef C, Burggraaf J, Vahrmeijer A . Fluorescence-guided surgery in colorectal cancer; A review on clinical results and future perspectives. Eur J Surg Oncol. 2021; 48(4):810-821. DOI: 10.1016/j.ejso.2021.10.005. View

11.

Hartung C, Porsch M, Stuckrath K, Kaufhold S, Staege M, Hanf V . Identifying High-Risk Triple-Negative Breast Cancer Patients by Molecular Subtyping. Breast Care (Basel). 2022; 16(6):637-647. PMC: 8740062. DOI: 10.1159/000519255. View

12.

Hendriks D, Pagliaro A, Andreatta F, Ma Z, van Giessen J, Massalini S . Human fetal brain self-organizes into long-term expanding organoids. Cell. 2024; 187(3):712-732.e38. DOI: 10.1016/j.cell.2023.12.012. View

13.

Jacob F, Salinas R, Zhang D, Nguyen P, Schnoll J, Wong S . A Patient-Derived Glioblastoma Organoid Model and Biobank Recapitulates Inter- and Intra-tumoral Heterogeneity. Cell. 2019; 180(1):188-204.e22. PMC: 7556703. DOI: 10.1016/j.cell.2019.11.036. View

14.

Koller M, Qiu S, Linssen M, Jansen L, Kelder W, De Vries J . Implementation and benchmarking of a novel analytical framework to clinically evaluate tumor-specific fluorescent tracers. Nat Commun. 2018; 9(1):3739. PMC: 6143516. DOI: 10.1038/s41467-018-05727-y. View

15.

Kunkele A, Taraseviciute A, Finn L, Johnson A, Berger C, Finney O . Preclinical Assessment of CD171-Directed CAR T-cell Adoptive Therapy for Childhood Neuroblastoma: CE7 Epitope Target Safety and Product Manufacturing Feasibility. Clin Cancer Res. 2016; 23(2):466-477. DOI: 10.1158/1078-0432.CCR-16-0354. View

16.

Lago C, Gianesello M, Santomaso L, Leva G, Ballabio C, Anderle M . Medulloblastoma and high-grade glioma organoids for drug screening, lineage tracing, co-culture and in vivo assay. Nat Protoc. 2023; 18(7):2143-2180. DOI: 10.1038/s41596-023-00839-2. View

17.

Lancaster M, Renner M, Martin C, Wenzel D, Bicknell L, Hurles M . Cerebral organoids model human brain development and microcephaly. Nature. 2013; 501(7467):373-9. PMC: 3817409. DOI: 10.1038/nature12517. View

18.

Lastowska M, Viprey V, Santibanez-Koref M, Wappler I, Peters H, Cullinane C . Identification of candidate genes involved in neuroblastoma progression by combining genomic and expression microarrays with survival data. Oncogene. 2007; 26(53):7432-44. DOI: 10.1038/sj.onc.1210552. View

19.

Massink M, Kooi I, van Mil S, Jordanova E, Ameziane N, Dorsman J . Proper genomic profiling of (BRCA1-mutated) basal-like breast carcinomas requires prior removal of tumor infiltrating lymphocytes. Mol Oncol. 2015; 9(4):877-88. PMC: 5528776. DOI: 10.1016/j.molonc.2014.12.012. View

20.

McCracken D, Schupper A, Lakomkin N, Malcolm J, Bray D, Hadjipanayis C . Turning on the light for brain tumor surgery: A 5-aminolevulinic acid story. Neuro Oncol. 2022; 24(Suppl 6):S52-S61. PMC: 9629477. DOI: 10.1093/neuonc/noac191. View