IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45775-1.html
   My bibliography  Save this article

Noncanonical function of folate through folate receptor 1 during neural tube formation

Author

Listed:
  • Olga A. Balashova

    (University of California Davis, School of Medicine)

  • Alexios A. Panoutsopoulos

    (University of California Davis, School of Medicine)

  • Olesya Visina

    (University of California Davis, School of Medicine)

  • Jacob Selhub

    (Tufts–USDA Human Nutrition Research Center on Aging)

  • Paul S. Knoepfler

    (University of California Davis, School of Medicine)

  • Laura N. Borodinsky

    (University of California Davis, School of Medicine)

Abstract

Folate supplementation reduces the occurrence of neural tube defects (NTDs), birth defects consisting in the failure of the neural tube to form and close. The mechanisms underlying NTDs and their prevention by folate remain unclear. Here we show that folate receptor 1 (FOLR1) is necessary for the formation of neural tube-like structures in human-cell derived neural organoids. FOLR1 knockdown in neural organoids and in Xenopus laevis embryos leads to NTDs that are rescued by pteroate, a folate precursor that is unable to participate in metabolism. We demonstrate that FOLR1 interacts with and opposes the function of CD2-associated protein, molecule essential for apical endocytosis and turnover of C-cadherin in neural plate cells. In addition, folates increase Ca2+ transient frequency, suggesting that folate and FOLR1 signal intracellularly to regulate neural plate folding. This study identifies a mechanism of action of folate distinct from its vitamin function during neural tube formation.

Suggested Citation

  • Olga A. Balashova & Alexios A. Panoutsopoulos & Olesya Visina & Jacob Selhub & Paul S. Knoepfler & Laura N. Borodinsky, 2024. "Noncanonical function of folate through folate receptor 1 during neural tube formation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45775-1
    DOI: 10.1038/s41467-024-45775-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45775-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45775-1?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. Phillippe Soubeyran & Katarzyna Kowanetz & Iwona Szymkiewicz & Wallace Y. Langdon & Ivan Dikic, 2002. "Erratum: Cbl–CIN85–endophilin complex mediates ligand-induced downregulation of EGF receptors," Nature, Nature, vol. 417(6884), pages 102-102, May.
    2. Madeline A. Lancaster & Magdalena Renner & Carol-Anne Martin & Daniel Wenzel & Louise S. Bicknell & Matthew E. Hurles & Tessa Homfray & Josef M. Penninger & Andrew P. Jackson & Juergen A. Knoblich, 2013. "Cerebral organoids model human brain development and microcephaly," Nature, Nature, vol. 501(7467), pages 373-379, September.
    3. Philippe Soubeyran & Katarzyna Kowanetz & Iwona Szymkiewicz & Wallace Y. Langdon & Ivan Dikic, 2002. "Cbl–CIN85–endophilin complex mediates ligand-induced downregulation of EGF receptors," Nature, Nature, vol. 416(6877), pages 183-187, March.
    4. Annalisa Petrelli & Giorgio F. Gilestro & Stefania Lanzardo & Paolo M. Comoglio & Nicola Migone & Silvia Giordano, 2002. "The endophilin–CIN85–Cbl complex mediates ligand-dependent downregulation of c-Met," Nature, Nature, vol. 416(6877), pages 187-190, March.
    5. Adam M. Session & Yoshinobu Uno & Taejoon Kwon & Jarrod A. Chapman & Atsushi Toyoda & Shuji Takahashi & Akimasa Fukui & Akira Hikosaka & Atsushi Suzuki & Mariko Kondo & Simon J. van Heeringen & Ian Qu, 2016. "Genome evolution in the allotetraploid frog Xenopus laevis," Nature, Nature, vol. 538(7625), pages 336-343, October.
    6. Chen Chen & Jiyuan Ke & X. Edward Zhou & Wei Yi & Joseph S. Brunzelle & Jun Li & Eu-Leong Yong & H. Eric Xu & Karsten Melcher, 2013. "Structural basis for molecular recognition of folic acid by folate receptors," Nature, Nature, vol. 500(7463), pages 486-489, August.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Ria S. Peesapati & Brianna L. Austin-Byler & Fathima Zahra Nawaz & Jonathan B. Stevenson & Stanelle A. Mais & Rabia N. Kaya & Michael G. Hassan & Nabraj Khanal & Alexandra C. Wells & Deena Ghiai & Ani, 2024. "A specific folate activates serotonergic neurons to control C. elegans behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    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. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    2. Camilla S. Colding-Christensen & Ellen S. Kakulidis & Javier Arroyo-Gomez & Ivo A. Hendriks & Connor Arkinson & Zita Fábián & Agnieszka Gambus & Niels Mailand & Julien P. Duxin & Michael L. Nielsen, 2023. "Profiling ubiquitin signalling with UBIMAX reveals DNA damage- and SCFβ-Trcp1-dependent ubiquitylation of the actin-organizing protein Dbn1," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    3. Elizabeth A. Werren & Geneva R. LaForce & Anshika Srivastava & Delia R. Perillo & Shaokun Li & Katherine Johnson & Safa Baris & Brandon Berger & Samantha L. Regan & Christian D. Pfennig & Sonja Munnik, 2024. "TREX tetramer disruption alters RNA processing necessary for corticogenesis in THOC6 Intellectual Disability Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    4. Wendiao Zhang & Ming Zhang & Zhenhong Xu & Hongye Yan & Huimin Wang & Jiamei Jiang & Juan Wan & Beisha Tang & Chunyu Liu & Chao Chen & Qingtuan Meng, 2023. "Human forebrain organoid-based multi-omics analyses of PCCB as a schizophrenia associated gene linked to GABAergic pathways," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. 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.
    6. Jessen V. Bredeson & Austin B. Mudd & Sofia Medina-Ruiz & Therese Mitros & Owen Kabnick Smith & Kelly E. Miller & Jessica B. Lyons & Sanjit S. Batra & Joseph Park & Kodiak C. Berkoff & Christopher Plo, 2024. "Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. 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.
    8. Maura Galimberti & Maria R. Nucera & Vittoria D. Bocchi & Paola Conforti & Elena Vezzoli & Matteo Cereda & Camilla Maffezzini & Raffaele Iennaco & Andrea Scolz & Andrea Falqui & Chiara Cordiglieri & M, 2024. "Huntington’s disease cellular phenotypes are rescued non-cell autonomously by healthy cells in mosaic telencephalic organoids," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Heiner Kuhl & Kang Du & Manfred Schartl & Lukáš Kalous & Matthias Stöck & Dunja K. Lamatsch, 2022. "Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    10. Tom Brandstätter & David B. Brückner & Yu Long Han & Ricard Alert & Ming Guo & Chase P. Broedersz, 2023. "Curvature induces active velocity waves in rotating spherical tissues," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    11. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Christina Kyrousi & Adam C. O’Neill & Agnieska Brazovskaja & Zhisong He & Pavel Kielkowski & Laure Coquand & Rossella Giaimo & Pierpaolo D’ Andrea & Alexander Belka & Andrea Forero Echeverry & Davide , 2021. "Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    13. Anthony K. Redmond & Dearbhaile Casey & Manu Kumar Gundappa & Daniel J. Macqueen & Aoife McLysaght, 2023. "Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. Teresa L. Rapp & Cole A. DeForest, 2023. "Tricolor visible wavelength-selective photodegradable hydrogel biomaterials," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    15. 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.
    16. Deborah Mesa & Elisa Barbieri & Andrea Raimondi & Stefano Freddi & Giorgia Miloro & Gorana Jendrisek & Giusi Caldieri & Micaela Quarto & Irene Schiano Lomoriello & Maria Grazia Malabarba & Arianna Bre, 2024. "A tripartite organelle platform links growth factor receptor signaling to mitochondrial metabolism," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Pamela E. Capendale & Inés García-Rodríguez & Anoop T. Ambikan & Lance A. Mulder & Josse A. Depla & Eline Freeze & Gerrit Koen & Carlemi Calitz & Vikas Sood & Renata Vieira de Sá & Ujjwal Neogi & Dasj, 2024. "Parechovirus infection in human brain organoids: host innate inflammatory response and not neuro-infectivity correlates to neurologic disease," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. Romain Beaubois & Jérémy Cheslet & Tomoya Duenki & Giuseppe De Venuto & Marta Carè & Farad Khoyratee & Michela Chiappalone & Pascal Branchereau & Yoshiho Ikeuchi & Timothée Levi, 2024. "BiœmuS: A new tool for neurological disorders studies through real-time emulation and hybridization using biomimetic Spiking Neural Network," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. 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.
    20. Betz, Ulrich A.K. & Arora, Loukik & Assal, Reem A. & Azevedo, Hatylas & Baldwin, Jeremy & Becker, Michael S. & Bostock, Stefan & Cheng, Vinton & Egle, Tobias & Ferrari, Nicola & Schneider-Futschik, El, 2023. "Game changers in science and technology - now and beyond," Technological Forecasting and Social Change, Elsevier, vol. 193(C).

    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_s41467-024-45775-1. 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.