LRP2 mediates folate uptake in the developing neural tube

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2261-2268

  Kur, Esther ^a,c   Mecklenburg, Nora ^a   Cabrera, Robert M ^b   Willnow, Thomas E ^a   Hammes, Annette ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Embryonic development; Endocytic receptor; Folate; Folate receptor; LRP2; Neural tube closure defects

Indexed keywords

FOLATE RECEPTOR 1; FOLIC ACID; MEGALIN; ALX3 PROTEIN, MOUSE; FOLR1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; LRP2 PROTEIN, MOUSE; REDUCED FOLATE CARRIER; SLC19A1 PROTEIN, MOUSE;

ADULT; ALX3 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; DRUG UPTAKE; EMBRYO; EMBRYO CULTURE; EMBRYONAL TISSUE; FOLATE METABOLISM; GENE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MOUSE; MOUSE EMBRYO; MUTANT; NEURAL TUBE; NEUROEPITHELIUM; NEURULATION; NONHUMAN; PRIORITY JOURNAL; REDUCTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; EMBRYOLOGY; ENDOCYTOSIS; GENETICS; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; ENDOCYTOSIS; FOLATE RECEPTOR 1; FOLIC ACID; HOMEODOMAIN PROTEINS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-2; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL TUBE; REDUCED FOLATE CARRIER PROTEIN;

EID: 84900790050     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.140145     Document Type: Article

References (38)

1. Birn, H., Zhai, X., Holm, J., Hansen, S. I., Jacobsen, C., Christensen, E. I. and Moestrup, S. K. (2005). Megalin binds and mediates cellular internalization of folate binding protein. FEBS J. 272, 4423-4430.
2. 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.
3. Cabrera, R. M., Hill, D. S., Etheredge, A. J. and Finnell, R. H. (2004). Investigations into the etiology of neural tube defects. Birth Defects Res. C Embryo Today 72, 330-344.
4. Cabrera, R. M., Shaw, G. M., Ballard, J. L., Carmichael, S. L., Yang, W., Lammer, E. J. and Finnell, R. H. (2008). Autoantibodies to folate receptor during pregnancy and neural tube defect risk. J. Reprod. Immunol. 79, 85-92.
5. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
6. Christ, A., Christa, A., Kur, E., Lioubinski, O., Bachmann, S., Willnow, T. E. and Hammes, A. (2012). LRP2 is an auxiliary SHH receptor required to condition the forebrain ventral midline for inductive signals. Dev. Cell 22, 268-278.
7. Christensen, E. I., Moskaug, J. O., Vorum, H., Jacobsen, C., Gundersen, T. E., Nykjaer, A., Blomhoff, R., Willnow, T. E. and Moestrup, S. K. (1999). Evidence for an essential role of megalin in transepithelial transport of retinol. J. Am. Soc. Nephrol. 10, 685-695.
8. Copp, A. J., Greene, N. D. and Murdoch, J. N. (2003). The genetic basis of mammalian neurulation. Nat. Rev. Genet. 4, 784-793.
9. Denz-Penhey, H. and Murdoch, J. C. (2009). A comparison between findings from the DREEM questionnaire and that from qualitative interviews. Med. Teach. 31, e449-e453.
10. 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.
11. Finnell, R. H., Blom, H. J. and Shaw, G. M. (2010). Does global hypomethylation contribute to susceptibility to neural tube defects? Am. J. Clin. Nutr. 91, 1153-1154.
12. Gelineau-van Waes, J., Heller, S., Bauer, L. K., Wilberding, J., Maddox, J. R., Aleman, F., Rosenquist, T. H. and Finnell, R. H. (2008a). Embryonic development in the reduced folate carrier knockout mouse is modulated by maternal folate supplementation. Birth Defects Res. A Clin. Mol. Teratol. 82, 494-507.
13. Gelineau-van Waes, J., Maddox, J. R., Smith, L. M., van Waes, M., Wilberding, J., Eudy, J. D., Bauer, L. K. and Finnell, R. H. (2008b). Microarray analysis of E9.5 reduced folate carrier (RFC1; Slc19a1) knockout embryos reveals altered expression of genes in the cubilin-megalin multiligand endocytic receptor complex. BMC Genomics 9, 156.
14. Gray, J. D., Nakouzi, G., Slowinska-Castaldo, B., Dazard, J. E., Rao, J. S., Nadeau, J. H. and Ross, M. E. (2010). Functional interactions between the LRP6 WNT co-receptor and folate supplementation. Hum. Mol. Genet. 19, 4560-4572.
15. Gray, J. D., Kholmanskikh, S., Castaldo, B. S., Hansler, A., Chung, H., Klotz, B., Singh, S., Brown, A. M. and Ross, M. E. (2013). LRP6 exerts non- canonical effects on Wnt signaling during neural tube closure. Hum. Mol. Genet. 22, 4267-4281.
16. Hammes, A., Guo, J. K., Lutsch, G., Leheste, J. R., Landrock, D., Ziegler, U., Gubler, M. C. and Schedl, A. (2001). Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 106, 319-329.
17. Hammes, A., Andreassen, T. K., Spoelgen, R., Raila, J., Hubner, N., Schulz, H., Metzger, J., Schweigert, F. J., Luppa, P. B., Nykjaer, A. et al. (2005). Role of endocytosis in cellular uptake of sex steroids. Cell 122, 751-762.
18. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
19. Harris, M. J. and Juriloff, D. M. (2010). An update to the list of mouse mutants with neural tube closure defects and advances toward a complete genetic perspective of neural tube closure. Birth Defects Res. A Clin. Mol. Teratol. 88, 653-669.
20. Horbinski, C., Kofler, J., Kelly, L. M., Murdoch, G. H. and Nikiforova, M. N. (2009). Diagnostic use of IDH1/2 mutation analysis in routine clinical testing of formalin-fixed, paraffin-embedded glioma tissues. J. Neuropathol. Exp. Neurol. 68, 1319-1325.
21. Kantarci, S., Al-Gazali, L., Hill, R. S., Donnai, D., Black, G. C., Bieth, E., Chassaing, N., Lacombe, D., Devriendt, K., Teebi, A. et al. (2007). Mutations in LRP2, which encodes the multiligand receptor megalin, cause Donnai-Barrow and facio-oculo-acoustico-renal syndromes. Nat. Genet. 39, 957-959.
22. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M. and Richardson, W. D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9, 173-179.
23. Lacey, S. W., Sanders, J. M., Rothberg, K. G., Anderson, R. G. and Kamen, B. A. (1989). Complementary DNA for the folate binding protein correctly predicts anchoring to the membrane by glycosyl-phosphatidylinositol. J. Clin. Invest. 84, 715-720.
24. Lakhwani, S., García-Sanz, P. and Vallejo, M. (2010). Alx3-deficient mice exhibit folic acid-resistant craniofacial midline and neural tube closure defects. Dev. Biol. 344, 869-880.
25. Mayor, S. and Riezman, H. (2004). Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell Biol. 5, 110-120.
26. Murdoch, J. N. and Copp, A. J. (2010). The relationship between sonic Hedgehog signaling, cilia, and neural tube defects. Birth Defects Res. A Clin. Mol. Teratol. 88, 633-652.
27. Nykjaer, A. and Willnow, T. E. (2002). The low-density lipoprotein receptor gene family: a cellular Swiss army knife? Trends Cell Biol. 12, 273-280.
28. Nykjaer, A., Dragun, D., Walther, D., Vorum, H., Jacobsen, C., Herz, J., Melsen, F., Christensen, E. I. and Willnow, T. E. (1999). An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 96, 507-515.
29. Piedrahita, J. A., Oetama, B., Bennett, G. D., van Waes, J., Kamen, B. A., Richardson, J., Lacey, S. W., Anderson, R. G. and Finnell, R. H. (1999). Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat. Genet. 23, 228-232.
30. Saito, A., Pietromonaco, S., Loo, A. K. and Farquhar, M. G. (1994). Complete cloning and sequencing of rat gp330/"megalin," a distinctive member of the low density lipoprotein receptor gene family. Proc. Natl. Acad. Sci. USA 91, 9725-9729.
31. Spiegelstein, O., Eudy, J. D. and Finnell, R. H. (2000). Identification of two putative novel folate receptor genes in humans and mouse. Gene 258, 117-125.
32. 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.
33. Spoelgen, R., Hammes, A., Anzenberger, U., Zechner, D., Andersen, O. M., Jerchow, B. and Willnow, T. E. (2005). LRP2/megalin is required for patterning of the ventral telencephalon. Development 132, 405-414.
34. Tang, L. S. and Finnell, R. H. (2003). Neural and orofacial defects in Folp1 knockout mice [corrected]. (corrected). Birth Defects Res. A Clin. Mol. Teratol. 67, 209-218.
35. Travers, D. A. and Haas, S. W. (2004). Evaluation of emergency medical text processor, a system for cleaning chief complaint text data. Acad. Emerg. Med. 11, 1170-1176.
36. 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.
37. Willnow, T. E., Hilpert, J., Armstrong, S. A., Rohlmann, A., Hammer, R. E., Burns, D. K. and Herz, J. (1996). Defective forebrain development in mice lacking gp330/megalin. Proc. Natl. Acad. Sci. USA 93, 8460-8464.
38. Zhao, R., Russell, R. G., Wang, Y., Liu, L., Gao, F., Kneitz, B., Edelmann, W. and Goldman, I. D. (2001). Rescue of embryonic lethality in reduced folate carrier-deficient mice by maternal folic acid supplementation reveals early neonatal failure of hematopoietic organs. J. Biol. Chem. 276, 10224-10228.