Plasma membrane cholesterol depletion disrupts prechordal plate and affects early forebrain patterning

Developmental Biology

Volumn 365, Issue 2, 2012, Pages 350-362

  Reis, Alice H ^a   Almeida Coburn, Karla L ^a   Louza, Mariana P ^a   Cerqueira, Débora M ^a   Aguiar, Diego P ^a   Silva Cardoso, Livia ^a   Mendes, Fábio A ^a   Andrade, Leonardo R ^a   Einicker Lamas, Marcelo ^a   Atella, Georgia C ^a   Brito, José M ^a   Abreu, José G ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Dkk; Head organizer; Lipid rafts; Methyl beta cyclodextrin; Microcephaly; Neutral lipids; Phospholipids

Indexed keywords

CHOLESTEROL; DICKKOPF 1 PROTEIN; METHYL BETA CYCLODEXTRIN;

ANIMAL TISSUE; ARTICLE; BLASTULA; CELL MEMBRANE; CELL STRUCTURE; CHICK; CHOLESTEROL RICH MEMBRANE MICRODOMAIN; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; EXPLANT; FOREBRAIN; GASTRULA; GENE EXPRESSION; LIPID COMPOSITION; NONHUMAN; PHENOTYPE; PRECHORDAL PLATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; XENOPUS;

ANIMALIA; ANURA;

EID: 84859973745     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.003     Document Type: Article

References (82)

1. Abreu J.G., Ketpura N.I., Reversade B., De Robertis E.M. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat. Cell Biol. 2002, 4:599-604.
2. -/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 1995, 121:3279-3290.
3. Adelmann H.B. The development of the prechordal plate and mesoderm of amblystoma punctatum. J. Morphol. 1932, 54:1-67.
4. Bauer M., Pelkmans L. A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett. 2006, 580:5559-5564.
5. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
6. Brito J.M., Teillet M.A., Le Douarin N.M. Induction of mirror-image supernumerary jaws in chicken mandibular mesenchyme by sonic hedgehog-producing cells. Development 2008, 135:2311-2319.
7. Brown D.A., London E. Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 1998, 164:103-114.
8. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 1992, 68:533-544.
9. Buschiazzo J., Bonini I.C., Alonso T.S. Inhibition of Bufo arenarum oocyte maturation induced by cholesterol depletion by methyl-beta-cyclodextrin. Role of low-density caveolae-like membranes. Biochim. Biophys. Acta 2008, 1778:1398-1406.
10. Camus A., Davidson B.P., Billiards S., Khoo P., Rivera-Perez J.A., Wakamiya M., Behringer R.R., Tam P.P. The morphogenetic role of midline mesendoderm and ectoderm in the development of the forebrain and the midbrain of the mouse embryo. Development 2000, 127:1799-1813.
11. Chapman S.C., Schubert F.R., Schoenwolf G.C., Lumsden A. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 2002, 245:187-199.
12. Chapman S.C., Schubert F.R., Schoenwolf G.C., Lumsden A. Anterior identity is established in chick epiblast by hypoblast and anterior definitive endoderm. Development 2003, 130:5091-5101.
13. Cho K.W., Blumberg B., Steinbeisser H., De Robertis E.M. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 1991, 67:1111-1120.
14. Cooper M.K., Wassif C.A., Krakowiak P.A., Taipale J., Gong R., Kelley R.I., Porter F.D., Beachy P.A. A defective response to hedgehog signaling in disorders of cholesterol biosynthesis. Nat. Genet. 2003, 33:508-513.
15. De Robertis E.M., Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 2004, 20:285-308.
16. De Robertis E.M., Larrain J., Oelgeschlager M., Wessely O. The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 2000, 1:171-181.
17. De Robertis E.M., Wessely O., Oelgeschlager M., Brizuela B., Pera E., Larrain J., Abreu J., Bachiller D. Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer. Int. J. Dev. Biol. 2001, 45:189-197.
18. Drab M., Verkade P., Elger M., Kasper M., Lohn M., Lauterbach B., Menne J., Lindschau C., Mende F., Luft F.C., Schedl A., Haller H., Kurzchalia T.V. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452.
19. Fang P.K., Solomon K.R., Zhuang L., Qi M., McKee M., Freeman M.R., Yelick P.C. Caveolin-1alpha and -1beta perform nonredundant roles in early vertebrate development. Am. J. Pathol. 2006, 169:2209-2222.
20. Fujimoto Y., Itabe H., Sakai J., Makita M., Noda J., Mori M., Higashi Y., Kojima S., Takano T. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim. Biophys. Acta 2004, 1644:47-59.
21. Galbiati F., Engelman J.A., Volonte D., Zhang X.L., Minetti C., Li M., Hou H., Kneitz B., Edelmann W., Lisanti M.P. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J. Biol. Chem. 2001, 276:21425-21433.
22. Garcia-Martinez V., Darnell D.K., Lopez-Sanchez C., Sosic D., Olson E.N., Schoenwolf G.C. State of commitment of prospective neural plate and prospective mesoderm in late gastrula/early neurula stages of avian embryos. Dev. Biol. 1997, 181:102-115.
23. Gaus K., Chklovskaia E., de St Fazekas, Groth B., Jessup W., Harder T. Condensation of the plasma membrane at the site of T lymphocyte activation. J. Cell Biol. 2005, 171:121-131.
24. Gerhart J. Evolution of the organizer and the chordate body plan. Int. J. Dev. Biol. 2001, 45:133-153.
25. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 1998, 391:357-362.
26. Harland R., Gerhart J. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 1997, 13:611-667.
27. Horwitz J., Perlman R.L. Measurement of inositol phospholipid metabolism in PC12 pheochromocytoma cells. Methods Enzymol. 1987, 141:169-175.
28. Jacobson K., Mouritsen O.G., Anderson R.G. Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 2007, 9:7-14.
29. Kazanskaya O., Glinka A., Niehrs C. The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning. Development 2000, 127:4981-4992.
30. Kiecker C., Niehrs C. The role of prechordal mesendoderm in neural patterning. Curr. Opin. Neurobiol. 2001, 11:27-33.
31. Kurth T. Immunocytochemistry of the amphibian embryo-from overview to ultrastructure. Int. J. Dev. Biol. 2003, 47:373-383.
32. Kurth T., Hausen P. Bottle cell formation in relation to mesodermal patterning in the Xenopus embryo. Mech. Dev. 2000, 97:117-131.
33. Kurzchalia T.V., Parton R.G. Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 1999, 11:424-431.
34. Lanoue L., Dehart D.B., Hinsdale M.E., Maeda N., Tint G.S., Sulik K.K. Limb, genital, CNS, and facial malformations result from gene/environment-induced cholesterol deficiency: further evidence for a link to sonic hedgehog. Am. J. Med. Genet. 1997, 73:24-31.
35. Larabell C.A., Torres M., Rowning B.A., Yost C., Miller J.R., Wu M., Kimelman D., Moon R.T. Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway. J. Cell Biol. 1997, 136:1123-1136.
36. Latinkic B.V., Smith J.C. Goosecoid and mix.1 repress Brachyury expression and are required for head formation in Xenopus. Development 1999, 126:1769-1779.
37. Lee J.D., Anderson K.V. Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn. 2008, 237:3464-3476.
38. Leung T., Bischof J., Soll I., Niessing D., Zhang D., Ma J., Jackle H., Driever W. bozozok directly represses bmp2b transcription and mediates the earliest dorsoventral asymmetry of bmp2b expression in zebrafish. Development 2003, 130:3639-3649.
39. Lingwood D., Simons K. Lipid rafts as a membrane-organizing principle. Science 2010, 327:46-50.
40. Lisanti M.P., Scherer P.E., Vidugiriene J., Tang Z., Hermanowski-Vosatka A., Tu Y.H., Cook R.F., Sargiacomo M. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J. Cell Biol. 1994, 126:111-126.
41. Liu P., Anderson R.G. Compartmentalized production of ceramide at the cell surface. J. Biol. Chem. 1995, 270:27179-27185.
42. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
43. Luria A., Vegelyte-Avery V., Stith B., Tsvetkova N.M., Wolkers W.F., Crowe J.H., Tablin F., Nuccitelli R. Detergent-free domain isolated from Xenopus egg plasma membrane with properties similar to those of detergent-resistant membranes. Biochemistry 2002, 41:13189-13197.
44. Magee T., Pirinen N., Adler J., Pagakis S.N., Parmryd I. Lipid rafts: cell surface platforms for T cell signaling. Biol. Res. 2002, 35:127-131.
45. Maxfield F.R. Plasma membrane microdomains. Curr. Opin. Cell Biol. 2002, 14:483-487.
46. Mes-Hartree M., Armstrong J.B. Lipid composition of developing Xenopus laevis embryos. Can. J. Biochem. 1976, 54:578-582.
47. Mo S., Wang L., Li Q., Li J., Li Y., Thannickal V.J., Cui Z. Caveolin-1 regulates dorsoventral patterning through direct interaction with beta-catenin in zebrafish. Dev. Biol. 2010, 344:210-223.
48. Niehrs C. Head in the WNT: the molecular nature of Spemann's head organizer. Trends Genet. 1999, 15:314-319.
49. Niehrs C. Regionally specific induction by the Spemann-Mangold organizer. Nat. Rev. Genet. 2004, 5:425-434.
50. Nieuwkoop P.D. The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Adv. Morphog. 1973, 10:1-39.
51. Nieuwkoop P.D., Farber J. Normal Table of Xenopis laevis (Daudin) 1967, North-Holland Publishing Co., Amsterdam, The Netherlands.
52. Nixon S.J., Carter A., Wegner J., Ferguson C., Floetenmeyer M., Riches J., Key B., Westerfield M., Parton R.G. Caveolin-1 is required for lateral line neuromast and notochord development. J. Cell Sci. 2007, 120:2151-2161.
53. Pandur P.D., Dirksen M.L., Moore K.B., Moody S.A. Xenopus flotillin1, a novel gene highly expressed in the dorsal nervous system. Dev. Dyn. 2004, 231:881-887.
54. Parton R.G. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J. Histochem. Cytochem. 1994, 42:155-166.
55. Parton R.G., Simons K. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 2007, 8:185-194.
56. Pierce S.K. Lipid rafts and B-cell activation. Nat. Rev. Immunol. 2002, 2:96-105.
57. Pike L.J., Miller J.M. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J. Biol. Chem. 1998, 273:22298-22304.
58. Prinetti A., Chigorno V., Tettamanti G., Sonnino S. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J. Biol. Chem. 2000, 275:11658-11665.
59. Racchi M., Baetta R., Salvietti N., Ianna P., Franceschini G., Paoletti R., Fumagalli R., Govoni S., Trabucchi M., Soma M. Secretory processing of amyloid precursor protein is inhibited by increase in cellular cholesterol content. Biochem. J. 1997, 322(Pt 3):893-898.
60. Radeva G., Sharom F.J. Isolation and characterization of lipid rafts with different properties from RBL-2H3 (rat basophilic leukaemia) cells. Biochem. J. 2004, 380:219-230.
61. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., Macaluso F., Russell R.G., Li M., Pestell R.G., Di Vizio D., Hou H., Kneitz B., Lagaud G., Christ G.J., Edelmann W., Lisanti M.P. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 2001, 276:38121-38138.
62. Razani B., Woodman S.E., Lisanti M.P. Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 2002, 54:431-467.
63. Reversade B., De Robertis E.M. Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 2005, 123:1147-1160.
64. Rizzo A.M., Gornati R., Galli C., Bernardini G., Berra B. Cholesterol, triacylglicerols and phospholipids during Xenopus embryo development. Cell Biol. Int. 1994, 18:1085-1090.
65. Roelink H., Nusse R. Expression of two members of the Wnt family during mouse development-restricted temporal and spatial patterns in the developing neural tube. Genes Dev. 1991, 5:381-388.
66. Roper K., Corbeil D., Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat. Cell Biol. 2000, 2:582-592.
67. Rothberg K.G., Heuser J.E., Donzell W.C., Ying Y.S., Glenney J.R., Anderson R.G. Caveolin, a protein component of caveolae membrane coats. Cell 1992, 68:673-682.
68. Ruiz J.I., Ochoa B. Quantification in the subnanomolar range of phospholipids and neutral lipids by monodimensional thin-layer chromatography and image analysis. J. Lipid Res. 1997, 38:1482-1489.
69. Ryu S.L., Fujii R., Yamanaka Y., Shimizu T., Yabe T., Hirata T., Hibi M., Hirano T. Regulation of dharma/bozozok by the Wnt pathway. Dev. Biol. 2001, 231:397-409.
70. Sargiacomo M., Sudol M., Tang Z., Lisanti M.P. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 1993, 122:789-807.
71. Sato K., Iwasaki T., Ogawa K., Konishi M., Tokmakov A.A., Fukami Y. Low density detergent-insoluble membrane of Xenopus eggs: subcellular microdomain for tyrosine kinase signaling in fertilization. Development 2002, 129:885-896.
72. Schneider S., Steinbeisser H., Warga R.M., Hausen P. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 1996, 57:191-198.
73. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
74. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1:31-39.
75. Spemann H. Embryonic Development and Induction 1938, Yale Univ Press.
76. Spemann H., Mangold H. Induction of embryonic primordia by implantation of organizers from a different species. Int. J. Dev. Biol. 1924, 45:13-38. Roux's Arch. Entw. Mech. 100:599-638. Reprinted and Transl.
77. Sulik K., Dehart D.B., Iangaki T., Carson J.L., Vrablic T., Gesteland K., Schoenwolf G.C. Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 1994, 201:260-278.
78. Tadjuidje E., Hollemann T. Cholesterol homeostasis in development: the role of Xenopus 7-dehydrocholesterol reductase (Xdhcr7) in neural development. Dev. Dyn. 2006, 235:2095-2110.
79. 2+ pump from proximal kidney tubules is exclusively localized and active in caveolae. FEBS Lett. 2004, 576:31-35.
80. Vereb G., Szollosi J., Matko J., Nagy P., Farkas T., Vigh L., Matyus L., Waldmann T.A., Damjanovich S. Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:8053-8058.
81. Wan H.C., Melo R.C., Jin Z., Dvorak A.M., Weller P.F. Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. FASEB J. 2007, 21:167-178.
82. Zlatkis A., Zak B., Boyle A.J. A new method for the direct determination of serum cholesterol. J. Lab. Clin. Med. 1953, 41:486-492.