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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
22 Feb 2024
Historique:
received: 29 11 2022
accepted: 02 02 2024
medline: 23 2 2024
pubmed: 23 2 2024
entrez: 22 2 2024
Statut: epublish

Résumé

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 Ca

Identifiants

pubmed: 38388461
doi: 10.1038/s41467-024-45775-1
pii: 10.1038/s41467-024-45775-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1642

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01NS105886
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
ID : R01NS113859
Organisme : National Science Foundation (NSF)
ID : 1754340
Organisme : Shriners Hospitals for Children
ID : 85111
Organisme : Shriners Hospitals for Children
ID : 84306

Informations de copyright

© 2024. The Author(s).

Références

Lyon, P., Strippoli, V., Fang, B. & Cimmino, L. B vitamins and one-carbon metabolism: implications in human health and disease. Nutrients 12, E2867 (2020).
Kancherla, V. et al. Preventing birth defects, saving lives, and promoting health equity: an urgent call to action for universal mandatory food fortification with folic acid. Lancet Glob. Health 10, e1053–e1057 (2022).
pubmed: 35617975
Wallingford, J. B., Niswander, L. A., Shaw, G. M. & Finnell, R. H. The continuing challenge of understanding, preventing, and treating neural tube defects. Science 339, 1222002 (2013).
pubmed: 23449594 pmcid: 3677196
Keuls, R. A., Finnell, R. H. & Parchem, R. J. Maternal metabolism influences neural tube closure. Trends Endocrinol. Metab. 34, 539–553 (2023).
pubmed: 37468429
Steele, J. W., Kim, S.-E. & Finnell, R. H. One-carbon metabolism and folate transporter genes: do they factor prominently in the genetic etiology of neural tube defects? Biochimie 173, 27–32 (2020).
pubmed: 32061804 pmcid: 7253344
Balashova, O. A., Visina, O. & Borodinsky, L. N. Folate action in nervous system development and disease. Dev. Neurobiol. 78, 391–402 (2018).
pubmed: 29380544 pmcid: 5867258
Newstead, S. Structural basis for recognition and transport of folic acid in mammalian cells. Curr. Opin. Struct. Biol. 74, 102353 (2022).
pubmed: 35303537 pmcid: 7612623
Zhao, R., Diop-Bove, N., Visentin, M. & Goldman, I. D. Mechanisms of membrane transport of folates into cells and across epithelia. Annu Rev. Nutr. 31, 177–201 (2011).
pubmed: 21568705
Alam, C. et al. Upregulation of reduced folate carrier by vitamin D enhances brain folate uptake in mice lacking folate receptor alpha. Proc. Natl Acad. Sci. USA 116, 17531–17540 (2019).
pubmed: 31405972 pmcid: 6717308
Nawaz, F. Z. & Kipreos, E. T. Emerging roles for folate receptor FOLR1 in signaling and cancer. Trends Endocrinol. Metab. 33, 159–174 (2022).
pubmed: 35094917 pmcid: 8923831
Boshnjaku, V. et al. Nuclear localization of folate receptor alpha: a new role as a transcription factor. Sci. Rep. 2, 980 (2012).
pubmed: 23243496 pmcid: 3522071
Chu, H. et al. Quantitative proteomics identifies FOLR1 to drive sorafenib resistance via activating autophagy in hepatocellular carcinoma cells. Carcinogenesis 42, 753–761 (2021).
pubmed: 33677528
Chaudhari, S. N. et al. Bacterial folates provide an exogenous signal for C. elegans germline stem cell proliferation. Dev. Cell 38, 33–46 (2016).
pubmed: 27404357 pmcid: 4958392
Machacek, C. et al. Folate receptor β regulates integrin CD11b/CD18 adhesion of a macrophage subset to collagen. J. Immunol. 197, 2229–2238 (2016).
pubmed: 27534550
Saitsu, H., Ishibashi, M., Nakano, H. & Shiota, K. Spatial and temporal expression offolate-binding protein 1 (Fbp1) is closely associated with anterior neural tube closure in mice. Dev. Dyn. 226, 112–117 (2003).
pubmed: 12508232
Balashova, O. A., Visina, O. & Borodinsky, L. N. Folate receptor 1 is necessary for neural plate cell apical constriction during Xenopus neural tube formation. Development 144, 1518–1530 (2017).
pubmed: 28255006 pmcid: 5399658
Piedrahita, J. A. et al. Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat. Genet. 23, 228–232 (1999).
pubmed: 10508523
Haigo, S. L., Hildebrand, J. D., Harland, R. M. & Wallingford, J. B. Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol. 13, 2125–2137 (2003).
pubmed: 14680628
Lee, J.-Y. & Harland, R. M. Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. Dev. Biol. 311, 40–52 (2007).
pubmed: 17868669 pmcid: 2744900
Hildebrand, J. D. Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 118, 5191–5203 (2005).
pubmed: 16249236
Lee, J.-Y. & Harland, R. M. Endocytosis is required for efficient apical constriction during Xenopus gastrulation. Curr. Biol. 20, 253–258 (2010).
pubmed: 20096583 pmcid: 3310928
Kowalczyk, I. et al. Neural tube closure requires the endocytic receptor Lrp2 and its functional interaction with intracellular scaffolds. Development 148, dev195008 (2021).
pubmed: 33500317 pmcid: 7860117
Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373–379 (2013).
pubmed: 23995685
Bonnard, C. et al. A loss-of-function NUAK2 mutation in humans causes anencephaly due to impaired Hippo-YAP signaling. J. Exp. Med. 217, e20191561 (2020).
pubmed: 32845958 pmcid: 7953732
Chen, C. et al. Structural basis for molecular recognition of folic acid by folate receptors. Nature 500, 486–489 (2013).
pubmed: 23851396 pmcid: 5797940
Nandadasa, S., Tao, Q., Menon, N. R., Heasman, J. & Wylie, C. N- and E-cadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136, 1327–1338 (2009).
pubmed: 19279134 pmcid: 2687464
De Beco, S., Gueudry, C., Amblard, F. & Coscoy, S. Endocytosis is required for E-cadherin redistribution at mature adherens junctions. Proc. Natl Acad. Sci. USA 106, 7010–7015 (2009).
pubmed: 19372377 pmcid: 2678428
Troyanovsky, R. B., Sokolov, E. P. & Troyanovsky, S. M. Endocytosis of cadherin from intracellular junctions is the driving force for cadherin adhesive dimer disassembly. MBoC 17, 3484–3493 (2006).
pubmed: 16760429 pmcid: 1525252
Su, W. & Kowalczyk, A. P. The VE-cadherin cytoplasmic domain undergoes proteolytic processing during endocytosis. Mol. Biol. Cell 28, 76–84 (2017).
pubmed: 27798242 pmcid: 5221631
Dustin, M. L. et al. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in t-cell contacts. Cell 94, 667–677 (1998).
pubmed: 9741631
Shih, N.-Y. et al. Congenital nephrotic syndrome in mice lacking CD2-associated protein. Science 286, 312–315 (1999).
pubmed: 10514378
Lynch, D. K. et al. A cortactin-CD2-associated protein (CD2AP) complex provides a novel link between epidermal growth factor receptor endocytosis and the actin cytoskeleton. J. Biol. Chem. 278, 21805–21813 (2003).
pubmed: 12672817
Kim, J. M. et al. CD2-associated protein haploinsufficiency is linked to glomerular disease susceptibility. Science 300, 1298–1300 (2003).
pubmed: 12764198
Petrelli, A. et al. The endophilin–CIN85–Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416, 187–190 (2002).
pubmed: 11894096
Soubeyran, P., Kowanetz, K., Szymkiewicz, I., Langdon, W. Y. & Dikic, I. Cbl–CIN85–endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416, 183–187 (2002).
pubmed: 11894095
Tossidou, I. et al. CD2AP regulates SUMOylation of CIN85 in podocytes. Mol. Cell Biol. 32, 1068–1079 (2012).
pubmed: 22203040 pmcid: 3295011
Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).
pubmed: 27762356 pmcid: 5313049
Bao, M. et al. CD2AP/SHIP1 complex positively regulates plasmacytoid dendritic cell receptor signaling by inhibiting the E3 ubiquitin ligase Cbl. J. Immunol. 189, 786–792 (2012).
pubmed: 22706086
Tsui, C. C. & Pierchala, B. A. CD2AP and Cbl-3/Cbl-c constitute a critical checkpoint in the regulation of ret signal transduction. J. Neurosci. 28, 8789–8800 (2008).
pubmed: 18753381 pmcid: 3844776
Calco, G. N., Stephens, O. R., Donahue, L. M., Tsui, C. C. & Pierchala, B. A. CD2-associated protein (CD2AP) enhances casitas B lineage lymphoma-3/c (Cbl-3/c)-mediated ret isoform-specific ubiquitination and degradation via its amino-terminal src homology 3 domains. J. Biol. Chem. 289, 7307–7319 (2014).
pubmed: 24425877 pmcid: 3953248
Fujita, Y. et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4, 222–231 (2002).
pubmed: 11836526
Christodoulou, N. & Skourides, P. A. Cell-autonomous Ca(2+) flashes elicit pulsed contractions of an apical actin network to drive apical constriction during neural tube closure. Cell Rep. 13, 2189–2202 (2015).
pubmed: 26673322
Sequerra, E. B., Goyal, R., Castro, P. A., Levin, J. B. & Borodinsky, L. N. NMDA receptor signaling is important for neural tube formation and for preventing antiepileptic drug-induced neural tube defects. J. Neurosci. 38, 4762–4773 (2018).
pubmed: 29712790 pmcid: 5956989
Moran, D. & Rice, R. W. Action of papaverine and ionophore A23187 on neurulation. Nature 261, 497–499 (1976).
pubmed: 778629
Ferreira, M. C. & Hilfer, S. R. Calcium regulation of neural fold formation: visualization of the actin cytoskeleton in living chick embryos. Dev. Biol. 159, 427–440 (1993).
pubmed: 8405669
Suzuki, M. et al. Distinct intracellular Ca2+ dynamics regulate apical constriction and differentially contribute to neural tube closure. Development dev.141952. https://doi.org/10.1242/dev.141952 . (2017).
Chen, J. et al. Disruption of the MacMARCKS gene prevents cranial neural tube closure and results in anencephaly. Proc. Natl Acad. Sci. USA 93, 6275–6279 (1996).
pubmed: 8692805 pmcid: 39012
Zanardelli, S., Christodoulou, N. & Skourides, P. A. Calpain2 protease: a new member of the Wnt/Ca2+ pathway modulating convergent extension movements in Xenopus. Dev. Biol. 384, 83–100 (2013).
pubmed: 24076278
Yaddanapudi, S. et al. CD2AP in mouse and human podocytes controls a proteolytic program that regulates cytoskeletal structure and cellular survival. J. Clin. Invest. 121, 3965–3980 (2011).
pubmed: 21911934 pmcid: 3195478
Bredemeyer, A. J. et al. The gastric epithelial progenitor cell niche and differentiation of the zymogenic (chief) cell lineage. Dev. Biol. 325, 211–224 (2009).
pubmed: 19013146
Tossidou, I. et al. Tyrosine phosphorylation of CD2AP affects stability of the slit diaphragm complex. JASN 30, 1220–1237 (2019).
pubmed: 31235616 pmcid: 6622410
Abdul-Wajid, S., Morales-Diaz, H., Khairallah, S. M. & Smith, W. C. T-type calcium channel regulation of neural tube closure and EphrinA/EPHA expression. Cell Rep. 13, 829–839 (2015).
pubmed: 26489462 pmcid: 4980084
Brown, J. M. & García-García, M. J. The secretory pathway calcium ATPase 1 (SPCA1) controls neural tube closure by regulating cytoskeletal dynamics. Development dev.170019. https://doi.org/10.1242/dev.170019 . (2018).
Singh, V. K., Munro, K. & Jia, Z. A novel calmodulin–β-PIX interaction and its implication in receptor tyrosine kinase regulation. Cell. Signal. 24, 1790–1796 (2012).
pubmed: 22588125
Wurster, B. & Schubiger, K. Oscillations and cell development in Dictyostelium discoideum stimulated by folic acid pulses. J. Cell Sci. 27, 105–114 (1977).
pubmed: 201655
Nebl, T. & Fisher, P. R. Intracellular Ca2+ signals in Dictyostelium chemotaxis are mediated exclusively by Ca2+ influx. J. Cell Sci. 110, 2845–2853 (1997).
pubmed: 9427292
McRobbie, S. J. & Newell, P. C. Changes in actin associated with the cytoskeleton following chemotactic stimulation of Dictyostelium discoideum. Biochem. Biophys. Res. Commun. 115, 351–359 (1983).
pubmed: 6311209
Nieuwkoop, P. D. & Faber, J. Normal Table of Xenopus Laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis. (Garland Pub., New York, 1994).
Lawe, D. C., Patki, V., Heller-Harrison, R., Lambright, D. & Corvera, S. The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. J. Biol. Chem. 275, 3699–3705 (2000).
pubmed: 10652369
Megason, S. G. In toto imaging of embryogenesis with confocal time-lapse microscopy. In Zebrafish (eds. Lieschke, G. J., Oates, A. C. & Kawakami, K.) vol. 546 317–332 (Humana Press, Totowa, NJ, 2009).
Namimatsu, S., Ghazizadeh, M. & Sugisaki, Y. Reversing the effects of formalin fixation with citraconic anhydride and heat: a universal antigen retrieval method. J. Histochem Cytochem. 53, 3–11 (2005).
pubmed: 15637333
Nesvizhskii, A. I., Keller, A., Kolker, E. & Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646–4658 (2003).
pubmed: 14632076
Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543–D552 (2022).
pubmed: 34723319
Chen, T.-W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).
pubmed: 23868258 pmcid: 3777791
Borodinsky, L. N. et al. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429, 523–530 (2004).
pubmed: 15175743
Swapna, I. & Borodinsky, L. N. Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation. Proc. Natl Acad. Sci. USA 109, 16336–16341 (2012).
pubmed: 22991474 pmcid: 3479614
Levin, J. B. & Borodinsky, L. N. Injury-induced Erk1/2 signaling tissue-specifically interacts with Ca2+ activity and is necessary for regeneration of spinal cord and skeletal muscle. Cell Calcium 102, 102540 (2022).
pubmed: 35074688 pmcid: 9542431
Zahn, N. et al. Normal Table of Xenopus development: a new graphical resource. Development 149, dev200356 (2022).
pubmed: 35833709 pmcid: 9445888

Auteurs

Olga A Balashova (OA)

Department of Physiology & Membrane Biology, Shriners Hospitals for Children Northern California, University of California Davis, School of Medicine, Sacramento, CA, 95817, USA. oabalashova@ucdavis.edu.

Alexios A Panoutsopoulos (AA)

Department of Physiology & Membrane Biology, Shriners Hospitals for Children Northern California, University of California Davis, School of Medicine, Sacramento, CA, 95817, USA.

Olesya Visina (O)

Department of Physiology & Membrane Biology, Shriners Hospitals for Children Northern California, University of California Davis, School of Medicine, Sacramento, CA, 95817, USA.

Jacob Selhub (J)

Tufts-USDA Human Nutrition Research Center on Aging, Boston, MA, USA.

Paul S Knoepfler (PS)

Department of Cell Biology & Human Anatomy, Shriners Hospitals for Children Northern California, University of California Davis, School of Medicine, Sacramento, CA, 95817, USA.

Laura N Borodinsky (LN)

Department of Physiology & Membrane Biology, Shriners Hospitals for Children Northern California, University of California Davis, School of Medicine, Sacramento, CA, 95817, USA. lnborodinsky@ucdavis.edu.

Classifications MeSH