Association of Engrailed homeoproteins with vesicles presenting caveolae-like properties

Development

Volumn 124, Issue 10, 1997, Pages 1865-1875

  Joliot, Alain ^a   Trembleau, Alain ^a   Raposo, Graça ^b   Calvet, Sophie ^a   Volovitch, Michel ^a   Prochiantz, Alain ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b INSTITUT CURIE   (France)

Author keywords

Caveolae; Cell fractionation; Engrailed; Homeoprotein; Microdomain; Neuron

Indexed keywords

CAVEOLIN; CELL MEMBRANE PROTEIN; CHOLERA TOXIN; CLATHRIN; GANGLIOSIDE GM1; GLYCOPROTEIN; HOMEODOMAIN PROTEIN; NERVE CELL ADHESION MOLECULE; NEUROMODULIN; SAPONIN; TRANSCRIPTION FACTOR; TRITON X 100;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CEREBELLUM; CHICKEN; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; MEMBRANE VESICLE; MESENCEPHALON; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; SOLUBILIZATION; SUCROSE GRADIENT;

ANIMALS; BRAIN; BRAIN CHEMISTRY; CAVEOLIN 1; CAVEOLINS; CELL COMPARTMENTATION; CELL NUCLEUS; CHICKENS; CHOLERA TOXIN; COS CELLS; CYTOPLASM; G(M1) GANGLIOSIDE; HOMEODOMAIN PROTEINS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICE; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; NEURONS; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RECEPTORS, CELL SURFACE; TRANSFECTION;

EID: 0030979030     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Akam, M. (1989). Hox and HOM: homologous gene clusters in insects and vertebrates. Cell 57, 347-349.
2. Bally-Cuif, L. and Wassef, M. (1995). Determination events in the nervous system of the vertebrate embryo. Curr. Opin. Genet. Dev. 5, 450-458.
3. Bedge, E. E., Hammang, J. P., Gribkoff, V. K. and Meiri, K. F. (1992). The role of GAP-43 in the molecular regulation of axon outgrowth and electrical excitability. Persp. Dev. Neurobiol. 1, 21-28.
4. Benowitz, L. and Routtenberg, A. (1987). A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity. Trends Neurosci. 10, 527-531.
5. Berlose, J., Convert, O., Derossi, D., Brunissen, A. and Chassaing, G. (1996). Conformational and associative behaviours of the third helix of antennapedia homeodomain in membrane-mimetic environments. Eur. J. Biochem. 242, 372-386.
6. Bloch-Gallego, E., Le Roux, I., Joliot, A. H., Volovitch, M., Henderson, C. E. and Prochiantz, A. (1993). Antennapedia homeobox peptide enhances growth and branching of embryonic chicken motoneurons in vitro. J. Cell Biol. 120, 485-492.
7. Bouillot, C., Prochiantz, A., Rougon, G. and Allinquant, B. (1996). Axonal amyloid precursor protein expressed by neurons in vitro is present in a membrane fraction with caveolae-like properties. J. Biol. Chem. 271, 7640-7644.
8. Briata, P., Di Blas, E., Gulisano, M., Mallamaci, A., Iannone, R., Boncinelli, E. and Corte, G. (1996). EMX1 homeoprotein is expressed in cell nuclei of the developing cerebal cortex and in the axons of the olfactory sensory neurons. Mech. Dev. 57, 169-180.
9. Chatelin, L., Volovitch, M., Joliot, A. H., Perez, F. and Prochiantz, A. (1996). Transcription factor Hoxa-5 is taken up by cells in culture and conveyed to their nuclei. Mech. Dev. 55, 111-117.
10. Conrad, P. A., Smart, E. J., Ying, Y.-S., Anderson, R. G. W. and Bloom, G. S. (1995). Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131, 1421-1433.
11. Derossi, D., Calvet, S., Trembleau, A., Brunissen, A., Chassaing, G. and Prochiantz, A. (1996). Cell internalization of the third helix of the antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271, 18188-18193.
12. Derossi, D., Joliot, A. H., Chassaing, G. and Prochiantz, A. (1994). The third helix of Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269, 10444-10450.
13. Doe, C. Q., Smouse, D. and Goodman, C. S. (1988). Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333, 376-378.
14. Dotti, C. G., Parton, R. G. and Simons, K. (1991). Polarized sorting of glypiated proteins in hippocampal neurons. Nature 349, 158-161.
15. Dotti, C. G. and Simons, K. (1990). Polarized sorting of viral glycoproteins to the axon and dendrites of hippocampal neurons in culture. Cell 62, 63-72.
16. Dubnau, J. and Struhl, G. (1996). RNA recognition and translational regulation by a homeodomain protein. Nature. 379, 694-699.
17. Evan, G. I., Lewis, G. K., Ramsay, G. and Bishop, J. M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616.
18. Faivre-Sarrailh, C., Gennarini, G., Goridis, C. and Rougon, G. (1992). F3/F11 cell surface molecule expression in the developing mouse cerebellum at synaptic sites and within granule cells. J. Neurosci. 12, 257-267.
19. Fra, A. M., Williamson, E., Simons, K. and Parton, R. G. (1995). De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Nat. Acad. Sci. USA 92, 8655-8659.
20. Gaunt, S. J., Sharpe, P. T. and Duboule, D. (1988). Spatially restricted domains of homeo-gene transcripts in mouse embryos: relation to a segmented body plan. Development 104, 169-179.
21. Gehring, W. J., Qian, Y. Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A. F., Resendez-Perez, D., Affolter, M., Otting, G. and Wüthrich, K. (1994). Homeodomain-DNA Recognition. Cell 78, 211-223.
22. Gennarini, G., Cibelli, C., Rougon, G., Mattei, M.-G. and Goridis, C. (1989). The mouse cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J. Cell Biol. 109, 775-788.
23. Gorodinsky, A. and Harris, D. A. (1995). Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin. J. Cell Biol. 129, 619-627.
24. Green, S., Issemann, I. and Sheer, E. (1988). A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 16, 369.
25. Joliot, A., Pernelle, C., Deagostini-Bazin, H. and Prochiantz, A. (1991a). Antennapedia homeobox peptide regulates neural morphogenesis. Proc. Nat. Acad. Sci. USA 88, 1864-1868.
26. Joliot, A. H., Triller, A., Volovitch, M., Pernelle, C. and Prochiantz, A. (1991b). α2,8-Polysialic acid is the neuronal surface receptor of Antennapedia homeobox peptide. The New Biologist 3, 1121-1134.
27. Joyner, A. L. (1996). Engrailed, Wnt and Pax genes regulate midbrain-hindbrain development. Trends Genet. 12, 15-20.
28. Keynes, R. and Krumlauf, R. (1994). Hox genes and regionalization of the nervous system. Annu. Rev. Neurosci. 17, 109-132.
29. Kleijmeer, M. J., Raposo, G. and Geuze, H. J. (1996). Characterization of MHC class II compartments by immunoelectron microscopy. METHODS: A Companion to Methods in Enzymology 10, 191-207.
30. Krämer, A., Haars, R., Kabisch, R., Will, H., Bautz, F.A., Bautz, E.K.F. (1980). Monoclonal antibody directed against RNA polymerase II of DM. Mol. Gen. Genet. 180, 193-199.
31. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
32. Kurzchalia, T. V., Dupree, P., Parton, R. G., Kellner, R., Virta, H., Lehnert, M. and Simons, K. (1992). VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J. Cell Biol. 118, 1003-1014.
33. Le Roux, I., Duharcourt, S., Volovitch, M., Prochiantz, A. and Ronchi, E. (1995). Promoter-specific regulation of genes expression by an exogenously added homeodomain that promotes neurite growth. FEBS Lett. 368, 311-314.
34. Le Roux, I., Joliot, A. H., Bloch-Gallego, E., Prochiantz, A. and Volovitch, M. (1993). Neurotrophic activity of the Antennapedia homeodomain depends on its specific DNA-binding properties. Proc. Nat. Acad. Sci. USA 90, 9120-9124.
35. Lucas, W. J., Bouché-Pillon, S., Jackson, D. P., Nguyen, L., Baker, L., Ding, B. and Hake, S. (1995). Selective trafficking of KNOTTED 1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980-1983.
36. Miller, D. M., Shen, M. M., Shamu, C. E., Bürglin, T. R., Ruvkin, G., Dubois, M. L., Ghee, M. and Wilson, L. (1992). C. elegans unc-4 gene encodes a homeoprotein that determines the pattern of synaptic input to specific motor neurons. Nature 355, 841-845.
37. Mohr, E. and Richter, D. (1992). Diversity of mRNAs in the axonal compartment of peptidergic neuron in the rat. Eur. J. Neurosci. 4, 870-876.
38. Parton, R. G. (1996). Caveolae and caveolins. Curr. Opin. Cell. Biol. 8, 542-548.
39. Patel, N. H., Martin-Blanco, E., Coleman, K. G., Poole, S. J., Ellis, M. C., Kornberg, T. B. and Goodman, C. S. (1989). Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58, 955-968.
40. Prochiantz, A. (1996). Getting hydrophilic compounds into cells: lessons from homeopeptides. Curr. Opin. Neurobiol. 6, 629-634.
41. Prochiantz, A. and Théodore, L. (1995). Nuclear/growth factors. BioEssays 17, 39-45.
42. Rijnboutt, S., Jansen, G., Posthuma, G., Hynes, J. B., Schornagel, J. H. and Strous, G. J. (1996). Endocytosis of GPI-linked membrane folate receptor-alpha. J. Cell Biol. 132, 35-47.
43. Rivera Pomar, R., Niessing, D., Schmidt, O. U., Gehring, W. J. and Jackle, H. (1996). RNA binding and translational suppression by bicoid. Nature 379, 746-749.
44. Rousselet, A., Autillo-Touati, A., Araud, D. and Prochiantz, A. (1990). In vitro regulation of neuronal morphogenesis and polarity by astrocyte-derived factors. Dev. Biol. 137, 33-45.
45. Rousselet, A., Fetler, L., Chamak, B. and Prochiantz, A. (1988). Rat mesencephalic neurons in culture exhibit different morphological traits in the presence of media conditioned on mesencephalic or striatal astroglia. Dev. Biol. 129, 495-504.
46. Rubenstein, J. R. and Puelles, L. (1994). Homeobox gene expression during development of the vertebrate brain. Curr. Top. Dev. Biol. 29, 1-65.
47. Scherer, P. E., Okamoto, T., Chun, M., Nishimoto, I., Lodish, H. F. and Lisanti, M. P. (1996). Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Prof. Nat. Acad. Sci. USA 93, 131-135.
48. Skene, J. H. P. and Virag, I. (1989). Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J. Cell Biol. 108, 613-624.
49. Smart, E., Ying, Y., Donzell, W. and Anderson, R. (1996). A Role for Caveolin in the Transport of Cholesterol from Endoplasmic Reticulum to Plama Membrane. J. Biol. Chem. 271, 29427-29435.
50. Song, K. S., Scherer, P. E., Tang, Z., Okamoto, T., Li, S., Chafel, M., Chu, C., Kohtz, D. S. and Lisanti, M. P. (1996). Expression of caveolin-3 in skeletal, cardiac and smooth muscle cells. J. Biol. Chem. 271, 15160-15165.
51. Tiedge, H., Zhou, A. and Brosius, N. A. T. (1993). Transport of BC1 RNA in hypothalamo-neurohypophyseal axons. J. Neurosci. 13, 4214-4219.
52. Trembleau, A., Morales, M. and Bloom, F. E. (1994). Aggregation of vasopressin mRNA in a subset of axonal swellings of the median eminence and posterior pituitary: light and electron microscopic evidence. J. Neurosci. 14, 39-53.
53. Vassar, R., Chao, S. K., Sitcheran, R., Nunez, J. M., Vosshall, L. B. and Axel, R. (1994). Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981-991.
54. White, J. G., Southgate, E. and Thomson, J. N. (1992). Mutations in Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons. Nature 355, 838-841.