Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures

Anna Urciuolo; Giovanni Giuseppe Giobbe; Yixiao Dong; Federica Michielin; Luca Brandolino; Michael Magnussen; Onelia Gagliano; Giulia Selmin; Valentina Scattolini; Paolo Raffa; Paola Caccin; Soichi Shibuya; Dominic Scaglioni; Xuechun Wang; Ju Qu; Marko Nikolic; Marco Montagner; Gabriel L Galea; Hans Clevers; Monica Giomo; Paolo De Coppi; Nicola Elvassore

doi:10.1038/s41467-023-37953-4

Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures

Anna Urciuolo, Giovanni Giuseppe Giobbe, Yixiao Dong, Federica Michielin, Luca Brandolino, Michael Magnussen, Onelia Gagliano, Giulia Selmin, Valentina Scattolini, Paolo Raffa, Paola Caccin, Soichi Shibuya, Dominic Scaglioni, Xuechun Wang, Ju Qu, Marko Nikolic, Marco Montagner, Gabriel L Galea, Hans Clevers, Monica GiomoPaolo De Coppi, Nicola Elvassore

Hubrecht Institute

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

51 Citaten (Scopus)

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Three-dimensional hydrogel-based organ-like cultures can be applied to study development, regeneration, and disease in vitro. However, the control of engineered hydrogel composition, mechanical properties and geometrical constraints tends to be restricted to the initial time of fabrication. Modulation of hydrogel characteristics over time and according to culture evolution is often not possible. Here, we overcome these limitations by developing a hydrogel-in-hydrogel live bioprinting approach that enables the dynamic fabrication of instructive hydrogel elements within pre-existing hydrogel-based organ-like cultures. This can be achieved by crosslinking photosensitive hydrogels via two-photon absorption at any time during culture. We show that instructive hydrogels guide neural axon directionality in growing organotypic spinal cords, and that hydrogel geometry and mechanical properties control differential cell migration in developing cancer organoids. Finally, we show that hydrogel constraints promote cell polarity in liver organoids, guide small intestinal organoid morphogenesis and control lung tip bifurcation according to the hydrogel composition and shape.

Originele taal-2	Engels
Pagina's (van-tot)	3128
Tijdschrift	Nature Communications
Volume	14
Nummer van het tijdschrift	1
DOI's	https://doi.org/10.1038/s41467-023-37953-4
Status	Gepubliceerd - 30 mei 2023

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10.1038/s41467-023-37953-4

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Urciuolo, A., Giobbe, G. G., Dong, Y., Michielin, F., Brandolino, L., Magnussen, M., Gagliano, O., Selmin, G., Scattolini, V., Raffa, P., Caccin, P., Shibuya, S., Scaglioni, D., Wang, X., Qu, J., Nikolic, M., Montagner, M., Galea, G. L., Clevers, H., ... Elvassore, N. (2023). Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures. Nature Communications, 14(1), 3128. https://doi.org/10.1038/s41467-023-37953-4

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title = "Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures",

abstract = "Three-dimensional hydrogel-based organ-like cultures can be applied to study development, regeneration, and disease in vitro. However, the control of engineered hydrogel composition, mechanical properties and geometrical constraints tends to be restricted to the initial time of fabrication. Modulation of hydrogel characteristics over time and according to culture evolution is often not possible. Here, we overcome these limitations by developing a hydrogel-in-hydrogel live bioprinting approach that enables the dynamic fabrication of instructive hydrogel elements within pre-existing hydrogel-based organ-like cultures. This can be achieved by crosslinking photosensitive hydrogels via two-photon absorption at any time during culture. We show that instructive hydrogels guide neural axon directionality in growing organotypic spinal cords, and that hydrogel geometry and mechanical properties control differential cell migration in developing cancer organoids. Finally, we show that hydrogel constraints promote cell polarity in liver organoids, guide small intestinal organoid morphogenesis and control lung tip bifurcation according to the hydrogel composition and shape.",

keywords = "Hydrogels/chemistry, Bioprinting, Organoids, Tissue Engineering/methods, Cell Polarity, Lung",

author = "Anna Urciuolo and Giobbe, {Giovanni Giuseppe} and Yixiao Dong and Federica Michielin and Luca Brandolino and Michael Magnussen and Onelia Gagliano and Giulia Selmin and Valentina Scattolini and Paolo Raffa and Paola Caccin and Soichi Shibuya and Dominic Scaglioni and Xuechun Wang and Ju Qu and Marko Nikolic and Marco Montagner and Galea, {Gabriel L} and Hans Clevers and Monica Giomo and {De Coppi}, Paolo and Nicola Elvassore",

note = "{\textcopyright} 2023. The Author(s).",

year = "2023",

month = may,

day = "30",

doi = "10.1038/s41467-023-37953-4",

language = "English",

volume = "14",

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Urciuolo, A, Giobbe, GG, Dong, Y, Michielin, F, Brandolino, L, Magnussen, M, Gagliano, O, Selmin, G, Scattolini, V, Raffa, P, Caccin, P, Shibuya, S, Scaglioni, D, Wang, X, Qu, J, Nikolic, M, Montagner, M, Galea, GL, Clevers, H, Giomo, M, De Coppi, P & Elvassore, N 2023, 'Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures', Nature Communications, vol. 14, nr. 1, blz. 3128. https://doi.org/10.1038/s41467-023-37953-4

TY - JOUR

T1 - Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures

AU - Urciuolo, Anna

AU - Giobbe, Giovanni Giuseppe

AU - Dong, Yixiao

AU - Michielin, Federica

AU - Brandolino, Luca

AU - Magnussen, Michael

AU - Gagliano, Onelia

AU - Selmin, Giulia

AU - Scattolini, Valentina

AU - Raffa, Paolo

AU - Caccin, Paola

AU - Shibuya, Soichi

AU - Scaglioni, Dominic

AU - Wang, Xuechun

AU - Qu, Ju

AU - Nikolic, Marko

AU - Montagner, Marco

AU - Galea, Gabriel L

AU - Clevers, Hans

AU - Giomo, Monica

AU - De Coppi, Paolo

AU - Elvassore, Nicola

PY - 2023/5/30

Y1 - 2023/5/30

N2 - Three-dimensional hydrogel-based organ-like cultures can be applied to study development, regeneration, and disease in vitro. However, the control of engineered hydrogel composition, mechanical properties and geometrical constraints tends to be restricted to the initial time of fabrication. Modulation of hydrogel characteristics over time and according to culture evolution is often not possible. Here, we overcome these limitations by developing a hydrogel-in-hydrogel live bioprinting approach that enables the dynamic fabrication of instructive hydrogel elements within pre-existing hydrogel-based organ-like cultures. This can be achieved by crosslinking photosensitive hydrogels via two-photon absorption at any time during culture. We show that instructive hydrogels guide neural axon directionality in growing organotypic spinal cords, and that hydrogel geometry and mechanical properties control differential cell migration in developing cancer organoids. Finally, we show that hydrogel constraints promote cell polarity in liver organoids, guide small intestinal organoid morphogenesis and control lung tip bifurcation according to the hydrogel composition and shape.

AB - Three-dimensional hydrogel-based organ-like cultures can be applied to study development, regeneration, and disease in vitro. However, the control of engineered hydrogel composition, mechanical properties and geometrical constraints tends to be restricted to the initial time of fabrication. Modulation of hydrogel characteristics over time and according to culture evolution is often not possible. Here, we overcome these limitations by developing a hydrogel-in-hydrogel live bioprinting approach that enables the dynamic fabrication of instructive hydrogel elements within pre-existing hydrogel-based organ-like cultures. This can be achieved by crosslinking photosensitive hydrogels via two-photon absorption at any time during culture. We show that instructive hydrogels guide neural axon directionality in growing organotypic spinal cords, and that hydrogel geometry and mechanical properties control differential cell migration in developing cancer organoids. Finally, we show that hydrogel constraints promote cell polarity in liver organoids, guide small intestinal organoid morphogenesis and control lung tip bifurcation according to the hydrogel composition and shape.

KW - Hydrogels/chemistry

KW - Bioprinting

KW - Organoids

KW - Tissue Engineering/methods

KW - Cell Polarity

KW - Lung

U2 - 10.1038/s41467-023-37953-4

DO - 10.1038/s41467-023-37953-4

M3 - Article

C2 - 37253730

SN - 2041-1723

VL - 14

SP - 3128

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures

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