A platform for efficient establishment and drug-response profiling of high-grade serous ovarian cancer organoids

Wojciech Senkowski; Laura Gall-Mas; Matías Marín Falco; Yilin Li; Kari Lavikka; Mette C Kriegbaum; Jaana Oikkonen; Daria Bulanova; Elin J Pietras; Karolin Voßgröne; Yan-Jun Chen; Erdogan Pekcan Erkan; Jun Dai; Anastasia Lundgren; Mia Kristine Grønning Høg; Ida Marie Larsen; Tarja Lamminen; Katja Kaipio; Jutta Huvila; Anni Virtanen; Lars Engelholm; Pernille Christiansen; Eric Santoni-Rugiu; Kaisa Huhtinen; Olli Carpén; Johanna Hynninen; Sampsa Hautaniemi; Anna Vähärautio; Krister Wennerberg

doi:10.1016/j.devcel.2023.04.012

A platform for efficient establishment and drug-response profiling of high-grade serous ovarian cancer organoids

Wojciech Senkowski^*, Laura Gall-Mas, Matías Marín Falco, Yilin Li, Kari Lavikka, Mette C Kriegbaum, Jaana Oikkonen, Daria Bulanova, Elin J Pietras, Karolin Voßgröne, Yan-Jun Chen, Erdogan Pekcan Erkan, Jun Dai, Anastasia Lundgren, Mia Kristine Grønning Høg, Ida Marie Larsen, Tarja Lamminen, Katja Kaipio, Jutta Huvila, Anni VirtanenLars Engelholm, Pernille Christiansen, Eric Santoni-Rugiu, Kaisa Huhtinen, Olli Carpén, Johanna Hynninen, Sampsa Hautaniemi, Anna Vähärautio, Krister Wennerberg^*

^*Corresponding author for this work

95 Citations (Scopus)

Abstract

The broad research use of organoids from high-grade serous ovarian cancer (HGSC) has been hampered by low culture success rates and limited availability of fresh tumor material. Here, we describe a method for generation and long-term expansion of HGSC organoids with efficacy markedly improved over previous reports (53% vs. 23%-38%). We established organoids from cryopreserved material, demonstrating the feasibility of using viably biobanked tissue for HGSC organoid derivation. Genomic, histologic, and single-cell transcriptomic analyses revealed that organoids recapitulated genetic and phenotypic features of original tumors. Organoid drug responses correlated with clinical treatment outcomes, although in a culture conditions-dependent manner and only in organoids maintained in human plasma-like medium (HPLM). Organoids from consenting patients are available to the research community through a public biobank and organoid genomic data are explorable through an interactive online tool. Taken together, this resource facilitates the application of HGSC organoids in basic and translational ovarian cancer research.

Original language	English
Journal	Developmental Cell
Volume	58
Issue number	12
Pages (from-to)	1106-1121.e7
ISSN	1534-5807
DOIs	https://doi.org/10.1016/j.devcel.2023.04.012
Publication status	Published - 19 Jun 2023

Keywords

Female
Genomics
Humans
Organoids/pathology
Ovarian Neoplasms/drug therapy
3D cell culture, culture conditions
high-grade serous ovarian cancer
organoids
HPLM
personalized medicine
functional precision medicine
scRNA-seq
organoid biobank
tumor models

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10.1016/j.devcel.2023.04.012

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Senkowski, W., Gall-Mas, L., Falco, M. M., Li, Y., Lavikka, K., Kriegbaum, M. C., Oikkonen, J., Bulanova, D., Pietras, E. J., Voßgröne, K., Chen, Y.-J., Erkan, E. P., Dai, J., Lundgren, A., Grønning Høg, M. K., Larsen, I. M., Lamminen, T., Kaipio, K., Huvila, J., ... Wennerberg, K. (2023). A platform for efficient establishment and drug-response profiling of high-grade serous ovarian cancer organoids. Developmental Cell, 58(12), 1106-1121.e7. https://doi.org/10.1016/j.devcel.2023.04.012

Senkowski, W, Gall-Mas, L, Falco, MM, Li, Y, Lavikka, K, Kriegbaum, MC, Oikkonen, J, Bulanova, D, Pietras, EJ, Voßgröne, K, Chen, Y-J, Erkan, EP, Dai, J, Lundgren, A, Grønning Høg, MK, Larsen, IM, Lamminen, T, Kaipio, K, Huvila, J, Virtanen, A, Engelholm, L, Christiansen, P, Santoni-Rugiu, E, Huhtinen, K, Carpén, O, Hynninen, J, Hautaniemi, S, Vähärautio, A & Wennerberg, K 2023, 'A platform for efficient establishment and drug-response profiling of high-grade serous ovarian cancer organoids', Developmental Cell, vol. 58, no. 12, pp. 1106-1121.e7. https://doi.org/10.1016/j.devcel.2023.04.012

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abstract = "The broad research use of organoids from high-grade serous ovarian cancer (HGSC) has been hampered by low culture success rates and limited availability of fresh tumor material. Here, we describe a method for generation and long-term expansion of HGSC organoids with efficacy markedly improved over previous reports (53\% vs. 23\%-38\%). We established organoids from cryopreserved material, demonstrating the feasibility of using viably biobanked tissue for HGSC organoid derivation. Genomic, histologic, and single-cell transcriptomic analyses revealed that organoids recapitulated genetic and phenotypic features of original tumors. Organoid drug responses correlated with clinical treatment outcomes, although in a culture conditions-dependent manner and only in organoids maintained in human plasma-like medium (HPLM). Organoids from consenting patients are available to the research community through a public biobank and organoid genomic data are explorable through an interactive online tool. Taken together, this resource facilitates the application of HGSC organoids in basic and translational ovarian cancer research.",

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AU - Senkowski, Wojciech

AU - Gall-Mas, Laura

AU - Falco, Matías Marín

AU - Li, Yilin

AU - Lavikka, Kari

AU - Kriegbaum, Mette C

AU - Oikkonen, Jaana

AU - Bulanova, Daria

AU - Pietras, Elin J

AU - Voßgröne, Karolin

AU - Chen, Yan-Jun

AU - Erkan, Erdogan Pekcan

AU - Dai, Jun

AU - Lundgren, Anastasia

AU - Grønning Høg, Mia Kristine

AU - Larsen, Ida Marie

AU - Lamminen, Tarja

AU - Kaipio, Katja

AU - Huvila, Jutta

AU - Virtanen, Anni

AU - Engelholm, Lars

AU - Christiansen, Pernille

AU - Santoni-Rugiu, Eric

AU - Huhtinen, Kaisa

AU - Carpén, Olli

AU - Hynninen, Johanna

AU - Hautaniemi, Sampsa

AU - Vähärautio, Anna

AU - Wennerberg, Krister

PY - 2023/6/19

Y1 - 2023/6/19

N2 - The broad research use of organoids from high-grade serous ovarian cancer (HGSC) has been hampered by low culture success rates and limited availability of fresh tumor material. Here, we describe a method for generation and long-term expansion of HGSC organoids with efficacy markedly improved over previous reports (53% vs. 23%-38%). We established organoids from cryopreserved material, demonstrating the feasibility of using viably biobanked tissue for HGSC organoid derivation. Genomic, histologic, and single-cell transcriptomic analyses revealed that organoids recapitulated genetic and phenotypic features of original tumors. Organoid drug responses correlated with clinical treatment outcomes, although in a culture conditions-dependent manner and only in organoids maintained in human plasma-like medium (HPLM). Organoids from consenting patients are available to the research community through a public biobank and organoid genomic data are explorable through an interactive online tool. Taken together, this resource facilitates the application of HGSC organoids in basic and translational ovarian cancer research.

AB - The broad research use of organoids from high-grade serous ovarian cancer (HGSC) has been hampered by low culture success rates and limited availability of fresh tumor material. Here, we describe a method for generation and long-term expansion of HGSC organoids with efficacy markedly improved over previous reports (53% vs. 23%-38%). We established organoids from cryopreserved material, demonstrating the feasibility of using viably biobanked tissue for HGSC organoid derivation. Genomic, histologic, and single-cell transcriptomic analyses revealed that organoids recapitulated genetic and phenotypic features of original tumors. Organoid drug responses correlated with clinical treatment outcomes, although in a culture conditions-dependent manner and only in organoids maintained in human plasma-like medium (HPLM). Organoids from consenting patients are available to the research community through a public biobank and organoid genomic data are explorable through an interactive online tool. Taken together, this resource facilitates the application of HGSC organoids in basic and translational ovarian cancer research.

KW - Female

KW - Genomics

KW - Humans

KW - Organoids/pathology

KW - Ovarian Neoplasms/drug therapy

KW - 3D cell culture, culture conditions

KW - high-grade serous ovarian cancer

KW - organoids

KW - HPLM

KW - personalized medicine

KW - functional precision medicine

KW - scRNA-seq

KW - organoid biobank

KW - tumor models

UR - https://www.scopus.com/pages/publications/85161580449

U2 - 10.1016/j.devcel.2023.04.012

DO - 10.1016/j.devcel.2023.04.012

M3 - Journal article

C2 - 37148882

SN - 1534-5807

VL - 58

SP - 1106-1121.e7

JO - Developmental Cell

JF - Developmental Cell

IS - 12

ER -

A platform for efficient establishment and drug-response profiling of high-grade serous ovarian cancer organoids

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Keywords

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