IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40006-5.html
   My bibliography  Save this article

Spatially controlled construction of assembloids using bioprinting

Author

Listed:
  • Julien G. Roth

    (Stanford University School of Medicine
    Stanford University
    Safety Assessment, Genentech Inc.)

  • Lucia G. Brunel

    (Stanford University)

  • Michelle S. Huang

    (Stanford University)

  • Yueming Liu

    (Stanford University)

  • Betty Cai

    (Stanford University)

  • Sauradeep Sinha

    (Stanford University)

  • Fan Yang

    (Stanford University
    Stanford University School of Medicine)

  • Sergiu P. Pașca

    (Stanford University
    Stanford University)

  • Sungchul Shin

    (Stanford University)

  • Sarah C. Heilshorn

    (Stanford University
    Stanford University)

Abstract

The biofabrication of three-dimensional (3D) tissues that recapitulate organ-specific architecture and function would benefit from temporal and spatial control of cell-cell interactions. Bioprinting, while potentially capable of achieving such control, is poorly suited to organoids with conserved cytoarchitectures that are susceptible to plastic deformation. Here, we develop a platform, termed Spatially Patterned Organoid Transfer (SPOT), consisting of an iron-oxide nanoparticle laden hydrogel and magnetized 3D printer to enable the controlled lifting, transport, and deposition of organoids. We identify cellulose nanofibers as both an ideal biomaterial for encasing organoids with magnetic nanoparticles and a shear-thinning, self-healing support hydrogel for maintaining the spatial positioning of organoids to facilitate the generation of assembloids. We leverage SPOT to create precisely arranged assembloids composed of human pluripotent stem cell-derived neural organoids and patient-derived glioma organoids. In doing so, we demonstrate the potential for the SPOT platform to construct assembloids which recapitulate key developmental processes and disease etiologies.

Suggested Citation

  • Julien G. Roth & Lucia G. Brunel & Michelle S. Huang & Yueming Liu & Betty Cai & Sauradeep Sinha & Fan Yang & Sergiu P. Pașca & Sungchul Shin & Sarah C. Heilshorn, 2023. "Spatially controlled construction of assembloids using bioprinting," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40006-5
    DOI: 10.1038/s41467-023-40006-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40006-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40006-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ashot S. Harutyunyan & Brian Krug & Haifen Chen & Simon Papillon-Cavanagh & Michele Zeinieh & Nicolas De Jay & Shriya Deshmukh & Carol C. L. Chen & Jad Belle & Leonie G. Mikael & Dylan M. Marchione & , 2019. "H3K27M induces defective chromatin spread of PRC2-mediated repressive H3K27me2/me3 and is essential for glioma tumorigenesis," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Fikri Birey & Jimena Andersen & Christopher D. Makinson & Saiful Islam & Wu Wei & Nina Huber & H. Christina Fan & Kimberly R. Cordes Metzler & Georgia Panagiotakos & Nicholas Thom & Nancy A. O’Rourke , 2017. "Assembly of functionally integrated human forebrain spheroids," Nature, Nature, vol. 545(7652), pages 54-59, May.
    3. Andrew C. Daly & Matthew D. Davidson & Jason A. Burdick, 2021. "3D bioprinting of high cell-density heterogeneous tissue models through spheroid fusion within self-healing hydrogels," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yanmei Zhang & Qifan Hu & Yuquan Pei & Hao Luo & Zixuan Wang & Xinxin Xu & Qing Zhang & Jianli Dai & Qianqian Wang & Zilian Fan & Yongcong Fang & Min Ye & Binhan Li & Mailin Chen & Qi Xue & Qingfeng Z, 2024. "A patient-specific lung cancer assembloid model with heterogeneous tumor microenvironments," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Anna Pagliaro & Roxy Finger & Iris Zoutendijk & Saskia Bunschuh & Hans Clevers & Delilah Hendriks & Benedetta Artegiani, 2023. "Temporal morphogen gradient-driven neural induction shapes single expanded neuroepithelium brain organoids with enhanced cortical identity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Tatsuya Osaki & Tomoya Duenki & Siu Yu A. Chow & Yasuhiro Ikegami & Romain Beaubois & Timothée Levi & Nao Nakagawa-Tamagawa & Yoji Hirano & Yoshiho Ikeuchi, 2024. "Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Yangteng Ou & Shixiang Cao & Yang Zhang & Hongjia Zhu & Chengzhi Guo & Wei Yan & Fengxue Xin & Weiliang Dong & Yanli Zhang & Masashi Narita & Ziyi Yu & Tuomas P. J. Knowles, 2023. "Bioprinting microporous functional living materials from protein-based core-shell microgels," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Augusto Faria Andrade & Alva Annett & Elham Karimi & Danai Georgia Topouza & Morteza Rezanejad & Yitong Liu & Michael McNicholas & Eduardo G. Gonzalez Santiago & Dhana Llivichuzhca-Loja & Arne Gehlhaa, 2024. "Immune landscape of oncohistone-mutant gliomas reveals diverse myeloid populations and tumor-promoting function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Lauren Rylaarsdam & Jennifer Rakotomamonjy & Eleanor Pope & Alicia Guemez-Gamboa, 2024. "iPSC-derived models of PACS1 syndrome reveal transcriptional and functional deficits in neuron activity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Elaine T. Lim & Yingleong Chan & Pepper Dawes & Xiaoge Guo & Serkan Erdin & Derek J. C. Tai & Songlei Liu & Julia M. Reichert & Mannix J. Burns & Ying Kai Chan & Jessica J. Chiang & Katharina Meyer & , 2022. "Orgo-Seq integrates single-cell and bulk transcriptomic data to identify cell type specific-driver genes associated with autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Tal Sharf & Tjitse Molen & Stella M. K. Glasauer & Elmer Guzman & Alessio P. Buccino & Gabriel Luna & Zhuowei Cheng & Morgane Audouard & Kamalini G. Ranasinghe & Kiwamu Kudo & Srikantan S. Nagarajan &, 2022. "Functional neuronal circuitry and oscillatory dynamics in human brain organoids," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    9. Yuanxiong Cao & Jiayi Tan & Haoran Zhao & Ting Deng & Yunxia Hu & Junhong Zeng & Jiawei Li & Yifan Cheng & Jiyuan Tang & Zhiwei Hu & Keer Hu & Bing Xu & Zitian Wang & Yaojiong Wu & Peter E. Lobie & Sh, 2022. "Bead-jet printing enabled sparse mesenchymal stem cell patterning augments skeletal muscle and hair follicle regeneration," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    10. Yueqi Wang & Simone Chiola & Guang Yang & Chad Russell & Celeste J. Armstrong & Yuanyuan Wu & Jay Spampanato & Paisley Tarboton & H. M. Arif Ullah & Nicolas U. Edgar & Amelia N. Chang & David A. Harmi, 2022. "Modeling human telencephalic development and autism-associated SHANK3 deficiency using organoids generated from single neural rosettes," Nature Communications, Nature, vol. 13(1), pages 1-25, December.
    11. Matthew A. Heinrich & Ricard Alert & Abraham E. Wolf & Andrej Košmrlj & Daniel J. Cohen, 2022. "Self-assembly of tessellated tissue sheets by expansion and collision," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    12. Chaitali Chakraborty & Itzel Nissen & Craig A. Vincent & Anna-Carin Hägglund & Andreas Hörnblad & Silvia Remeseiro, 2023. "Rewiring of the promoter-enhancer interactome and regulatory landscape in glioblastoma orchestrates gene expression underlying neurogliomal synaptic communication," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Ariane Lismer & Sarah Kimmins, 2023. "Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    14. Maisumu Gulimiheranmu & Shuang Li & Junmei Zhou, 2021. "In Vitro Recapitulation of Neuropsychiatric Disorders with Pluripotent Stem Cells-Derived Brain Organoids," IJERPH, MDPI, vol. 18(23), pages 1-14, November.
    15. Fabio Papes & Antonio P. Camargo & Janaina S. Souza & Vinicius M. A. Carvalho & Ryan A. Szeto & Erin LaMontagne & José R. Teixeira & Simoni H. Avansini & Sandra M. Sánchez-Sánchez & Thiago S. Nakahara, 2022. "Transcription Factor 4 loss-of-function is associated with deficits in progenitor proliferation and cortical neuron content," Nature Communications, Nature, vol. 13(1), pages 1-26, December.
    16. Sungjin Min & Suran Kim & Woo-Sup Sim & Yi Sun Choi & Hyebin Joo & Jae-Hyun Park & Su-Jin Lee & Hyeok Kim & Mi Jeong Lee & Inhea Jeong & Baofang Cui & Sung-Hyun Jo & Jin-Ju Kim & Seok Beom Hong & Yeon, 2024. "Versatile human cardiac tissues engineered with perfusable heart extracellular microenvironment for biomedical applications," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40006-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.