Folate receptor 1 is necessary for neural plate cell apical constriction during Xenopus neural tube formation

Development (Cambridge)

Volumn 144, Issue 8, 2017, Pages 1518-1530

  Balashova, Olga A ^a   Visina, Olesya ^a   Borodinsky, Laura N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Folate receptor; Folic acid; Neural tube defects; Xenopus

Indexed keywords

FOLATE RECEPTOR 1; FOLIC ACID; METHOTREXATE; CADHERIN; MORPHOLINO OLIGONUCLEOTIDE; XENOPUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APICAL MEMBRANE; ARTICLE; CELL SHAPE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE SILENCING; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NEURAL TUBE DEFECT; NEUROECTODERM; NEURULATION; NONHUMAN; PRIORITY JOURNAL; XENOPUS LAEVIS; ANIMAL; CELL POLARITY; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; HUMAN; METABOLISM; NONMAMMALIAN EMBRYO; ORGANOGENESIS;

ANIMALS; CADHERINS; CELL POLARITY; CELL SHAPE; EMBRYO, NONMAMMALIAN; ENDOCYTOSIS; FEMALE; FOLATE RECEPTOR 1; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GENE TARGETING; HUMANS; MORPHOLINOS; NEURAL PLATE; NEURAL TUBE; NEURULATION; ORGANOGENESIS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 85017523139     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.137315     Document Type: Article

References (77)

1. Afman, L. A., Blom, H. J., Van der Put, N. M. J. and Van Straaten, H.W. M. (2003). Homocysteine interference in neurulation: a chick embryo model. Birth Defects Res. A Clin. Mol. Teratol 67, 421-428.
2. Afman, L. A., Blom, H. J., Drittij, M.-J., Brouns, M. R. and van Straaten, H.W. M. (2005). Inhibition of transmethylation disturbs neurulation in chick embryos. Brain Res. Dev. Brain Res. 158, 59-65.
3. Antony, A. C. (1992). The biological chemistry of folate receptors. Blood 79, 2807-2820.
4. Antony, A. C. (1996). Folate receptors. Annu. Rev. Nutr. 16, 501-521.
5. Barber, R. C., Bennett, G. D., Greer, K. A. and Finnell, R. H. (1999). Expression patterns of folate binding proteins one and two in the developing mouse embryo. Mol. Genet. Metab. 66, 31-39.
6. Belgacem, Y. H. and Borodinsky, L. N. (2011). Sonic hedgehog signaling is decoded by calcium spike activity in the developing spinal cord. Proc. Natl. Acad. Sci. USA 108, 4482-4487.
7. Belgacem, Y. H. and Borodinsky, L. N. (2015). Inversion of Sonic hedgehog action on its canonical pathway by electrical activity. Proc. Natl. Acad. Sci. USA 112, 4140-4145.
8. Blom, H. J., Shaw, G. M., den Heijer, M. and Finnell, R. H. (2006). Neural tube defects and folate: case far from closed. Nat. Rev. Neurosci. 7, 724-731.
9. Borodinsky, L. N., Root, C. M., Cronin, J. A., Sann, S. B., Gu, X. and Spitzer, N. C. (2004). Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429, 523-530.
10. Burkel, B. M., von Dassow, G. and Bement, W. M. (2007). Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton 64, 822-832.
11. Chen, Z., Karaplis, A. C., Ackerman, S. L., Pogribny, I. P., Melnyk, S., Lussier-Cacan, S., Chen, M. F., Pai, A., John, S. W., Smith, R. S. et al. (2001). Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum. Mol. Genet. 10, 433-443.
12. Colas, J.-F. and Schoenwolf, G. C. (2001). Towards a cellular and molecular understanding of neurulation. Dev. Dyn. 221, 117-145.
13. Davidson, L. A. and Keller, R. E. (1999). Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension. Development 126, 4547-4556.
14. Detrait, E. R., George, T. M., Etchevers, H. C., Gilbert, J. R., Vekemans, M. and Speer, M. C. (2005). Human neural tube defects: developmental biology, epidemiology, and genetics. Neurotoxicol. Teratol. 27, 515-524.
15. Elwood, P. C. (1989). Molecular cloning and characterization of the human folatebinding protein cDNA from placenta and malignant tissue culture (KB) cells. J. Biol. Chem. 264, 14893-14901.
16. Eom, D. S., Amarnath, S., Fogel, J. L. and Agarwala, S. (2011). Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway. Development 138, 3179-3188.
17. Finnell, R. H., Spiegelstein, O., Wlodarczyk, B., Triplett, A., Pogribny, I. P., Melnyk, S. and James, J. S. (2002). DNA methylation in Folbp1 knockout mice supplemented with folic acid during gestation. J. Nutr. 132, 2457S-2461S.
18. Girotto, F., Scott, L., Avchalumov, Y., Harris, J., Iannattone, S., Drummond- Main, C., Tobias, R., Bello-Espinosa, L., Rho, J. M., Davidsen, J. et al. (2013). High dose folic acid supplementation of rats alters synaptic transmission and seizure susceptibility in offspring. Sci. Rep. 3, 1465.
19. Grem, J. L., Voeller, D. M., Geoffroy, F., Horak, E., Johnston, P. G. and Allegra, C. J. (1994). Determinants of trimetrexate lethality in human colon cancer cells. Br. J. Cancer 70, 1075-1084.
20. Haigo, S. L., Hildebrand, J. D., Harland, R. M. and Wallingford, J. B. (2003). Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol. 13, 2125-2137.
21. Harris, W. A. and Hartenstein, V. (1991). Neuronal determination without cell division in Xenopus embryos. Neuron 6, 499-515.
22. Heffer-Lauc, M., Viljetic, B., Vajn, K., Schnaar, R. L. and Lauc, G. (2007). Effects of detergents on the redistribution of gangliosides and GPI-anchored proteins in brain tissue sections. J. Histochem. Cytochem. 55, 805-812.
23. Hensey, C. and Gautier, J. (1998). Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev. Biol. 203, 36-48.
24. Hildebrand, J. D. and Soriano, P. (1999). Shroom, a PDZ domain-containing actinbinding protein, is required for neural tube morphogenesis in mice. Cell 99, 485-497.
25. Holm, J., Hansen, S. I., Hoier-Madsen, M. and Bostad, L. (1991). High-affinity folate binding in human choroid plexus. Characterization of radioligand binding, immunoreactivity, molecular heterogeneity and hydrophobic domain of the binding protein. Biochem. J. 280, 267-271.
26. Hook, K. E., Nelson, J. M., Roberts, B. J., Griswold, D. P. and Leopold, W. R. (1986). Cell cycle effects of trimetrexate (CI-898). Cancer Chemother. Pharmacol. 16, 116-120.
27. Iskandar, B. J., Rizk, E., Meier, B., Hariharan, N., Bottiglieri, T., Finnell, R. H., Jarrard, D. F., Banerjee, R. V., Skene, J. H., Nelson, A. et al. (2010). Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J. Clin. Invest. 120, 1603-1616.
28. Jarrett, O., Stow, J. L., Yap, A. S. and Key, B. (2002). Dynamin-dependent endocytosis is necessary for convergent-extension movements in Xenopus animal cap explants. Int. J. Dev. Biol. 46, 467-473.
29. Jolivet, J., Cowan, K. H., Curt, G. A., Clendeninn, N. J. and Chabner, B. A. (1983). The pharmacology and clinical use of methotrexate. N. Engl. J. Med. 309, 1094-1104.
30. Kee, N., Wilson, N., De Vries, M., Bradford, D., Key, B. and Cooper, H. M. (2008). Neogenin and RGMa control neural tube closure and neuroepithelial morphology by regulating cell polarity. J. Neurosci. 28, 12643-12653.
31. Keller, R., Shih, J., Sater, A. K. and Moreno, C. (1992). Planar induction of convergence and extension of the neural plate by the organizer of Xenopus. Dev. Dyn. 193, 218-234.
32. Klein, S. L., Strausberg, R. L., Wagner, L., Pontius, J., Clifton, S. W. and Richardson, P. (2002). Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Dev. Dyn. 225, 384-391.
33. Koch, M. C., Stegmann, K., Ziegler, A., Schröter, B. and Ermert, A. (1998). Evaluation of the MTHFR C677T allele and the MTHFR gene locus in a German spina bifida population. Eur. J. Pediatr. 157, 487-492.
34. Kozak, M. (1987a). An analysis of 5’-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15, 8125-8148.
35. Kozak, M. (1987b). At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196, 947-950.
36. Lee, J.-Y. and Harland, R. M. (2010). Endocytosis is required for efficient apical constriction during Xenopus gastrulation. Curr. Biol. 20, 253-258.
37. Matsuda, T. and Cepko, C. L. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA 104, 1027-1032.
38. Meuli, M. and Moehrlen, U. (2014). Fetal surgery for myelomeningocele is effective: a critical look at the whys. Pediatr. Surg. Int. 30, 689-697.
39. Moody, S. A. (1987). Fates of the blastomeres of the 16-cell stage Xenopus embryo. Dev. Biol. 119, 560-578.
40. Morita, H., Nandadasa, S., Yamamoto, T. S., Terasaka-Iioka, C., Wylie, C. and Ueno, N. (2010). Nectin-2 and N-cadherin interact through extracellular domains and induce apical accumulation of F-actin in apical constriction of Xenopus neural tube morphogenesis. Development 137, 1315-1325.
41. Mornet, E., Muller, F., Lenvoisé-Furet, A., Delezoide, A. L., Col, J. Y., Simon-Bouy, B. and Serre, J.-L. (1997). Screening of the C677T mutation on the methylenetetrahydrofolate reductase gene in French patients with neural tube defects. Hum. Genet. 100, 512-514.
42. Moury, J. D. and Schoenwolf, G. C. (1995). Cooperative model of epithelial shaping and bending during avian neurulation: autonomous movements of the neural plate, autonomous movements of the epidermis, and interactions in the neural plate/epidermis transition zone. Dev. Dyn. 204, 323-337.
43. MRC Vitamin Study Research Group (1991). Prevention of neural tube defects: results of the medical research council vitamin study. Lancet 338, 131-137.
44. Mu, F.-T., Callaghan, J. M., Steele-Mortimer, O., Stenmark, H., Parton, R. G., Campbell, P. L., McCluskey, J., Yeo, J.-P., Tock, E. P. and Toh, B.-H. (1995). EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine “fingers” and contains a calmodulin-binding IQ motif. J. Biol. Chem. 270, 13503-13511.
45. Namimatsu, S., Ghazizadeh, M. and Sugisaki, Y. (2005). Reversing the effects of formalin fixation with citraconic anhydride and heat: a universal antigen retrieval method. J. Histochem. Cytochem. 53, 3-11.
46. Nandadasa, S., Tao, Q., Menon, N. R., Heasman, J. and Wylie, C. (2009). 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.
47. Nieuwkoop, P. D. and Faber, J. (1994). Normal Table of Xenopus Laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg Till the End of Metamorphosis. New York: Garland Pub.
48. Nishimura, T. and Takeichi, M. (2008). Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502.
49. Nishimura, T. and Takeichi, M. (2009). Remodeling of the adherens junctions during morphogenesis. Curr. Top. Dev. Biol. 89, 33-54.
50. O’Byrne, M. R., Au, K. S., Morrison, A. C., Lin, J.-I., Fletcher, J. M., Ostermaier, K. K., Tyerman, G. H., Doebel, S. and Northrup, H. (2010). Association of folate receptor (FOLR1, FOLR2, FOLR3) and reduced folate carrier (SLC19A1) genes with meningomyelocele. Birth Defects Res. A Clin. Mol. Teratol 88, 689-694.
51. Ossipova, O., Kim, K., Lake, B. B., Itoh, K., Ioannou, A. and Sokol, S. Y. (2014). Role of Rab11 in planar cell polarity and apical constriction during vertebrate neural tube closure. Nat. Commun. 5, 3734.
52. Papapetrou, C., Lynch, S. A., Burn, J. and Edwards, Y. H. (1996). Methylenetetrahydrofolate reductase and neural tube defects. Lancet 348, 58.
53. Piedrahita, J. A., Oetama, B., Bennett, G. D., van Waes, J., Kamen, B. A., Richardson, J., Lacey, S. W., Anderson, R. G. W. and Finnell, R. H. (1999). Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat. Genet. 23, 228-232.
54. Pitkin, R. M. (2007). Folate and neural tube defects. Am. J. Clin. Nutr. 85, 285S-288S.
55. Prasad, P. D., Ramamoorthy, S., Moe, A. J., Smith, C. H., Leibach, F. H. and Ganapathy, V. (1994). Selective expression of the high-affinity isoform of the folate receptor (FR-alpha) in the human placental syncytiotrophoblast and choriocarcinoma cells. Biochim. Biophys. Acta 1223, 71-75.
56. Ramaekers, V. T., Rothenberg, S. P., Sequeira, J. M., Opladen, T., Blau, N., Quadros, E. V. and Selhub, J. (2005). Autoantibodies to folate receptors in the cerebral folate deficiency syndrome. N. Engl. J. Med. 352, 1985-1991.
57. Saitsu, H., Ishibashi, M., Nakano, H. and Shiota, K. (2003). Spatial and temporal expression of folate-binding protein 1 (Fbp1) is closely associated with anterior neural tube closure in mice. Dev. Dyn. 226, 112-117.
58. Schoenwolf, G. C. (1988). Microsurgical analyses of avian neurulation: separation of medial and lateral tissues. J. Comp. Neurol. 276, 498-507.
59. Schoenwolf, G. C., Everaert, S., Bortier, H. and Vakaet, L. (1989). Neural plateand neural tube-forming potential of isolated epiblast areas in avian embryos. Anat. Embryol. (Berl) 179, 541-549.
60. Selhub, J. and Franklin, W. A. (1984). The folate-binding protein of rat kidney. Purification, properties, and cellular distribution. J. Biol. Chem. 259, 6601-6606.
61. Sequeira, J. M., Desai, A., Berrocal-Zaragoza, M. I., Murphy, M. M., Fernandez- Ballart, J. D. and Quadros, E. V. (2016). Exposure to folate receptor alpha antibodies during gestation and weaning leads to severe behavioral deficits in rats: a pilot study. PLoS ONE 11, e0152249.
62. Sirotnak, F. M. and Tolner, B. (1999). Carrier-mediated membrane transport of folates in mammalian cells. Annu. Rev. Nutr. 19, 91-122.
63. Smithells, R.W., Sheppard, S. and Schorah, C. J. (1976). Vitamin dificiencies and neural tube defects. Arch. Dis. Child. 51, 944-950.
64. Speer, M. C., Worley, G., Mackey, J. F., Melvin, E., Oakes, W. J. and George, T. M. (1997). The thermolabile variant of methylenetetrahydrofolate reductase (MTHFR) is not a major risk factor for neural tube defect in American Caucasians. The NTD Collaborative Group. Neurogenetics 1, 149-150.
65. Spiegelstein, O., Mitchell, L. E., Merriweather, M. Y., Wicker, N. J., Zhang, Q., Lammer, E. J. and Finnell, R. H. (2004). Embryonic development of folate binding protein-1 (Folbp1) knockout mice: Effects of the chemical form, dose, and timing of maternal folate supplementation. Dev. Dyn. 231, 221-231.
66. Sugimoto, K., Okabayashi, K., Sedohara, A., Hayata, T. and Asashima, M. (2007). The role of XBtg2 in Xenopus neural development. Dev. Neurosci. 29, 468-479.
67. Swanson, D. A., Liu, M.-L., Baker, P. J., Garrett, L., Stitzel, M., Wu, J., Harris, M., Banerjee, R., Shane, B. and Brody, L. C. (2001). Targeted disruption of the methionine synthase gene in mice. Mol. Cell. Biol. 21, 1058-1065.
68. Swapna, I. and Borodinsky, L. N. (2012). Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation. Proc. Natl. Acad. Sci. USA 109, 16336-16341.
69. Tu, M. K. and Borodinsky, L. N. (2014). Spontaneous calcium transients manifest in the regenerating muscle and are necessary for skeletal muscle replenishment. Cell Calcium 56, 34-41.
70. van der Put, N. M. J., Steegers-Theunissen, R. P., Frosst, P., Trijbels, F. J., Eskes, T. K., van den Heuvel, L. P., Mariman, E. C., den Heyer, M., Rozen, R. and Blom, H. J. (1995). Mutated methylenetetrahydrofolate reductase as a risk factor for spina bifida. Lancet 346, 1070-1071.
71. van der Put, N. M., van den Heuvel, L. P., Steegers-Theunissen, R. P., Trijbels, F. J., Eskes, T. K., Mariman, E. C., den Heyer, M. and Blom, H. J. (1996). Decreased methylene tetrahydrofolate reductase activity due to the 677C–>T mutation in families with spina bifida offspring. J. Mol. Med. (Berl.) 74, 691-694.
72. Wallingford, J. B. and Harland, R. M. (2002). Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 129, 5815-5825.
73. Wallingford, J. B., Niswander, L. A., Shaw, G. M. and Finnell, R. H. (2013). The continuing challenge of understanding, preventing, and treating neural tube defects. Science 339, 1222002.
74. Watanabe, M., Osada, J., Aratani, Y., Kluckman, K., Reddick, R., Malinow, M. R. and Maeda, N. (1995). Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia. Proc. Natl. Acad. Sci. USA 92, 1585-1589.
75. West, J. J. and Harris, T. J. C. (2016). Cadherin trafficking for tissue morphogenesis: control and consequences. Traffic 17, 1233-1243.
76. Wilcken, D. E. L. and Wang, X. L. (1996). Relevance to spina bifida of mutated methylenetetrahydrofolate reductase. Lancet 347, 340.
77. Zimmerman, J., Selhub, J. and Rosenberg, I. H. (1987). Competitive inhibition of folate absorption by dihydrofolate reductase inhibitors, trimethoprim and pyrimethamine. Am. J. Clin. Nutr. 46, 518-522.