IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47166-y.html
   My bibliography  Save this article

Lineage specific transcription factor waves reprogram neuroblastoma from self-renewal to differentiation

Author

Listed:
  • Deblina Banerjee

    (National Cancer Institute)

  • Sukriti Bagchi

    (National Cancer Institute)

  • Zhihui Liu

    (National Cancer Institute)

  • Hsien-Chao Chou

    (National Cancer Institute)

  • Man Xu

    (National Cancer Institute)

  • Ming Sun

    (National Cancer Institute)

  • Sara Aloisi

    (Case Western Reserve University
    University of Bologna)

  • Zalman Vaksman

    (New York Genome Center)

  • Sharon J. Diskin

    (Perelman School of Medicine)

  • Mark Zimmerman

    (Dana-Farber Cancer Institute)

  • Javed Khan

    (National Cancer Institute)

  • Berkley Gryder

    (Case Western Reserve University)

  • Carol J. Thiele

    (National Cancer Institute)

Abstract

Temporal regulation of super-enhancer (SE) driven transcription factors (TFs) underlies normal developmental programs. Neuroblastoma (NB) arises from an inability of sympathoadrenal progenitors to exit a self-renewal program and terminally differentiate. To identify SEs driving TF regulators, we use all-trans retinoic acid (ATRA) to induce NB growth arrest and differentiation. Time-course H3K27ac ChIP-seq and RNA-seq reveal ATRA coordinated SE waves. SEs that decrease with ATRA link to stem cell development (MYCN, GATA3, SOX11). CRISPR-Cas9 and siRNA verify SOX11 dependency, in vitro and in vivo. Silencing the SOX11 SE using dCAS9-KRAB decreases SOX11 mRNA and inhibits cell growth. Other TFs activate in sequential waves at 2, 4 and 8 days of ATRA treatment that regulate neural development (GATA2 and SOX4). Silencing the gained SOX4 SE using dCAS9-KRAB decreases SOX4 expression and attenuates ATRA-induced differentiation genes. Our study identifies oncogenic lineage drivers of NB self-renewal and TFs critical for implementing a differentiation program.

Suggested Citation

  • Deblina Banerjee & Sukriti Bagchi & Zhihui Liu & Hsien-Chao Chou & Man Xu & Ming Sun & Sara Aloisi & Zalman Vaksman & Sharon J. Diskin & Mark Zimmerman & Javed Khan & Berkley Gryder & Carol J. Thiele, 2024. "Lineage specific transcription factor waves reprogram neuroblastoma from self-renewal to differentiation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47166-y
    DOI: 10.1038/s41467-024-47166-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47166-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47166-y?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. Sharon J. Diskin & Cuiping Hou & Joseph T. Glessner & Edward F. Attiyeh & Marci Laudenslager & Kristopher Bosse & Kristina Cole & Yaël P. Mossé & Andrew Wood & Jill E. Lynch & Katlyn Pecor & Maura Dia, 2009. "Copy number variation at 1q21.1 associated with neuroblastoma," Nature, Nature, vol. 459(7249), pages 987-991, June.
    2. Bieke Decaesteker & Geertrui Denecker & Christophe Van Neste & Emmy M. Dolman & Wouter Van Loocke & Moritz Gartlgruber & Carolina Nunes & Fanny De Vloed & Pauline Depuydt & Karen Verboom & Dries Romba, 2018. "TBX2 is a neuroblastoma core regulatory circuitry component enhancing MYCN/FOXM1 reactivation of DREAM targets," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    3. Derek A. Oldridge & Andrew C. Wood & Nina Weichert-Leahey & Ian Crimmins & Robyn Sussman & Cynthia Winter & Lee D. McDaniel & Maura Diamond & Lori S. Hart & Shizhen Zhu & Adam D. Durbin & Brian J. Abr, 2015. "Genetic predisposition to neuroblastoma mediated by a LMO1 super-enhancer polymorphism," Nature, Nature, vol. 528(7582), pages 418-421, December.
    4. Lu Wang & Tze King Tan & Adam D. Durbin & Mark W. Zimmerman & Brian J. Abraham & Shi Hao Tan & Phuong Cao Thi Ngoc & Nina Weichert-Leahey & Koshi Akahane & Lee N. Lawton & Jo Lynne Rokita & John M. Ma, 2019. "ASCL1 is a MYCN- and LMO1-dependent member of the adrenergic neuroblastoma core regulatory circuitry," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    5. Zhihui Liu & Xiyuan Zhang & Haiyan Lei & Norris Lam & Sakereh Carter & Oliver Yockey & Max Xu & Arnulfo Mendoza & Edjay R. Hernandez & Jun S. Wei & Javed Khan & Marielle E. Yohe & Jack F. Shern & Caro, 2020. "CASZ1 induces skeletal muscle and rhabdomyosarcoma differentiation through a feed-forward loop with MYOD and MYOG," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    6. Svetlana O. Dodonova & Fangjie Zhu & Christian Dienemann & Jussi Taipale & Patrick Cramer, 2020. "Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function," Nature, Nature, vol. 580(7805), pages 669-672, April.
    7. Charles Y. Lin & Serap Erkek & Yiai Tong & Linlin Yin & Alexander J. Federation & Marc Zapatka & Parthiv Haldipur & Daisuke Kawauchi & Thomas Risch & Hans-Jörg Warnatz & Barbara C. Worst & Bensheng Ju, 2016. "Active medulloblastoma enhancers reveal subgroup-specific cellular origins," Nature, Nature, vol. 530(7588), pages 57-62, February.
    8. Kai Wang & Sharon J. Diskin & Haitao Zhang & Edward F. Attiyeh & Cynthia Winter & Cuiping Hou & Robert W. Schnepp & Maura Diamond & Kristopher Bosse & Patrick A. Mayes & Joseph Glessner & Cecilia Kim , 2011. "Integrative genomics identifies LMO1 as a neuroblastoma oncogene," Nature, Nature, vol. 469(7329), pages 216-220, January.
    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. Bieke Decaesteker & Amber Louwagie & Siebe Loontiens & Fanny De Vloed & Sarah-Lee Bekaert & Juliette Roels & Suzanne Vanhauwaert & Sara De Brouwer & Ellen Sanders & Alla Berezovskaya & Geertrui Deneck, 2023. "SOX11 regulates SWI/SNF complex components as member of the adrenergic neuroblastoma core regulatory circuitry," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Cécile Thirant & Agathe Peltier & Simon Durand & Amira Kramdi & Caroline Louis-Brennetot & Cécile Pierre-Eugène & Margot Gautier & Ana Costa & Amandine Grelier & Sakina Zaïdi & Nadège Gruel & Irène Ji, 2023. "Reversible transitions between noradrenergic and mesenchymal tumor identities define cell plasticity in neuroblastoma," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Shigekazu Murakami & Shannon M. White & Alec T. McIntosh & Chan D. K. Nguyen & Chunling Yi, 2023. "Spontaneously evolved progenitor niches escape Yap oncogene addiction in advanced pancreatic ductal adenocarcinomas," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Lễ B Nguyễn & Sharon J Diskin & Mario Capasso & Kai Wang & Maura A Diamond & Joseph Glessner & Cecilia Kim & Edward F Attiyeh & Yael P Mosse & Kristina Cole & Achille Iolascon & Marcella Devoto & Hako, 2011. "Phenotype Restricted Genome-Wide Association Study Using a Gene-Centric Approach Identifies Three Low-Risk Neuroblastoma Susceptibility Loci," PLOS Genetics, Public Library of Science, vol. 7(3), pages 1-9, March.
    5. Hsiao-Yun Chen & Yavuz T. Durmaz & Yixiang Li & Amin H. Sabet & Amir Vajdi & Thomas Denize & Emily Walton & Yasmin Nabil Laimon & John G. Doench & Navin R. Mahadevan & Julie-Aurore Losman & David A. B, 2022. "Regulation of neuroendocrine plasticity by the RNA-binding protein ZFP36L1," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    6. Marios G. Koliopoulos & Reyhan Muhammad & Theodoros I. Roumeliotis & Fabienne Beuron & Jyoti S. Choudhary & Claudio Alfieri, 2022. "Structure of a nucleosome-bound MuvB transcription factor complex reveals DNA remodelling," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Jin-Lin Cao & Ping Yuan & Abudumailamu Abuduwufuer & Wang Lv & Yun-Hai Yang & Jian Hu, 2015. "Association between the TERT Genetic Polymorphism rs2853676 and Cancer Risk: Meta-Analysis of 76 108 Cases and 134 215 Controls," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-14, June.
    8. Min Kyung Lee & Nasim Azizgolshani & Joshua A. Shapiro & Lananh N. Nguyen & Fred W. Kolling & George J. Zanazzi & Hildreth Robert Frost & Brock C. Christensen, 2024. "Identifying tumor type and cell type-specific gene expression alterations in pediatric central nervous system tumors," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Royce W. Zhou & Jia Xu & Tiphaine C. Martin & Alexis L. Zachem & John He & Sait Ozturk & Deniz Demircioglu & Ankita Bansal & Andrew P. Trotta & Bruno Giotti & Berkley Gryder & Yao Shen & Xuewei Wu & S, 2022. "A local tumor microenvironment acquired super-enhancer induces an oncogenic driver in colorectal carcinoma," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    10. Keun-Woo Lee & So-Young Yeo & Jeong-Ryeol Gong & Ok-Jae Koo & Insuk Sohn & Woo Yong Lee & Hee Cheol Kim & Seong Hyeon Yun & Yong Beom Cho & Mi-Ae Choi & Sugyun An & Juhee Kim & Chang Ohk Sung & Kwang-, 2022. "PRRX1 is a master transcription factor of stromal fibroblasts for myofibroblastic lineage progression," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    11. Gerard Llimos & Vincent Gardeux & Ute Koch & Judith F. Kribelbauer & Antonina Hafner & Daniel Alpern & Joern Pezoldt & Maria Litovchenko & Julie Russeil & Riccardo Dainese & Riccardo Moia & Abdurraouf, 2022. "A leukemia-protective germline variant mediates chromatin module formation via transcription factor nucleation," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    12. Luca Pagliaroli & Patrizia Porazzi & Alyxandra T. Curtis & Chiara Scopa & Harald M. M. Mikkers & Christian Freund & Lucia Daxinger & Sandra Deliard & Sarah A. Welsh & Sarah Offley & Connor A. Ott & Br, 2021. "Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    13. Ting Shen & Ting Ni & Jiaxuan Chen & Haitao Chen & Xiaopin Ma & Guangwen Cao & Tianzhi Wu & Haisheng Xie & Bin Zhou & Gang Wei & Hexige Saiyin & Suqin Shen & Peng Yu & Qianyi Xiao & Hui Liu & Yuzheng , 2022. "An enhancer variant at 16q22.1 predisposes to hepatocellular carcinoma via regulating PRMT7 expression," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Tyler M. Weaver & Nicole M. Hoitsma & Jonah J. Spencer & Lokesh Gakhar & Nicholas J. Schnicker & Bret D. Freudenthal, 2022. "Structural basis for APE1 processing DNA damage in the nucleosome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    15. Sveinn Bjarnason & Jordan A. P. McIvor & Andreas Prestel & Kinga S. Demény & Jakob T. Bullerjahn & Birthe B. Kragelund & Davide Mercadante & Pétur O. Heidarsson, 2024. "DNA binding redistributes activation domain ensemble and accessibility in pioneer factor Sox2," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    16. Noha A. M. Shendy & Melissa Bikowitz & Logan H. Sigua & Yang Zhang & Audrey Mercier & Yousef Khashana & Stephanie Nance & Qi Liu & Ian M. Delahunty & Sarah Robinson & Vanshita Goel & Matthew G. Rees &, 2024. "Group 3 medulloblastoma transcriptional networks collapse under domain specific EP300/CBP inhibition," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Yichen Zhong & Hakimeh Moghaddas Sani & Bishnu P. Paudel & Jason K. K. Low & Ana P. G. Silva & Stefan Mueller & Chandrika Deshpande & Santosh Panjikar & Xavier J. Reid & Max J. Bedward & Antoine M. Oi, 2022. "The role of auxiliary domains in modulating CHD4 activity suggests mechanistic commonality between enzyme families," Nature Communications, Nature, vol. 13(1), pages 1-17, 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:15:y:2024:i:1:d:10.1038_s41467-024-47166-y. 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.