Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1

Journal of Cell Biology

Volumn 176, Issue 4, 2007, Pages 483-495

  Dubreuil, Véronique ^a,c   Marzesco, Anne Marie ^a   Corbeil, Denis ^b   Huttner, Wieland B ^a   Wilsch Bräuninger, Michaela ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b Biotec   (Germany)

^c ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; PROMININ 1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; EUKARYOTIC FLAGELLUM; NEURAL TUBE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ANIMALS; ANTIGENS, CD; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL DIVISION; CELL MEMBRANE; CELL PROLIFERATION; CELLS, CULTURED; CHICK EMBRYO; CILIA; CYTOKINESIS; EPITHELIAL CELLS; EXTRACELLULAR SPACE; GLYCOPROTEINS; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONS; PEPTIDES; PROTEIN TRANSPORT; STEM CELLS;

MAMMALIA;

EID: 33847005413     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200608137     Document Type: Article

References (68)

1. Aaku-Saraste, E., B. Oback, A. Hellwig, and W.B. Huttner. 1997. Neuroepithelial cells downregulate their plasma membrane polarity prior to neural tube closure and neurogenesis. Mech. Dev. 69:71-81.
2. Allenspach, A.L., and L.E. Roth. 1967. Structural variations during mitosis in the chick embryo. J. Cell Biol. 33:179-196.
3. Bancroft, M., and R. Bellairs. 1975. Differentiation of the neural plate and neural tube in the young chick embryo. A study by scanning and transmission electron microscopy. Anat. Embryol. (Berl.). 147:309-335.
4. Beaudoin, A.R., and G. Grondin. 1991. Shedding of vesicular material from the cell surface of eukaryotic cells: different cellular phenomena. Biochim. Biophys. Acta. 1071:203-219.
5. Bellairs, R., and M. Bancroft. 1975. Midbodies and beaded threads. Am. J. Anat. 143:393-398.
6. Bergman, K., U.W. Goodenough, D.A. Goodenough, J. Jawitz, and H. Martin. 1975. Gametic differentiation in Chlamydomonas reinhardtii. II. Flagellar membranes and the agglutination reaction. J. Cell Biol. 67:606-622.
7. Buck, R.C., and J.M. Tidsale. 1962a. An electron microscopic study of the cleavage furrow in mammalian cells. J. Cell Biol. 13:117-125.
8. Buck, R.C., and J.M. Tisdale. 1962b. The fine structure of the mid-body of the rat erythroblast. J. Cell Biol. 13:109-115.
9. Campbell, R.E., O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias, and R.Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
10. Chenn, A., and S.K. McConnell. 1995. Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell. 82:631-641.
11. Cohen, E., S. Binet, and V. Meininger. 1988. Ciliogenesis and centriole formation in the mouse embryonic nervous system. An ultrastructural analysis. Biol. Cell. 62:165-169.
12. Corbeil, D., K. Röper, C.A. Fargeas, A. Joester, and W.B. Huttner. 2001. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2:82-91.
13. Drake, C.J., P.A. Fleming, A.C. Larue, J.L. Barth, M.R. Chintalapudi, and W.S. Argraves. 2004. Differential distribution of cubilin and megalin expression in the mouse embryo. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 277:163-170.
14. Fargeas, C.A., D. Corbeil, and W.B. Huttner. 2003. AC133 antigen, CD133, prominin-1, prominin-2, etc.: prominin family gene products in need of a rational nomenclature. Stem Cells. 21:506-508.
15. Fargeas, C.A., A.-V. Fonseca, W.B. Huttner, and D. Corbeil. 2006. Prominin-1 (CD133): from progenitor cells to human diseases. Future Lipidology. 1:213-225.
16. Field, C.M., and B.M. Alberts. 1995. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131:165-178.
17. Février, B., and G. Raposo. 2004. Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 16:415-421.
18. Glotzer, M. 2001. Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17:351-386.
19. Golsteyn, R.M., S.J. Schultz, J. Bartek, A. Ziemiecki, T. Ried, and E.A. Nigg. 1994. Cell cycle analysis and chromosomal localization of human Plk1, a putative homologue of the mitotic kinases Drosophila polo and Saccharomyces cerevisiae Cdc5. J. Cell Sci. 107:1509-1517.
20. Goodenough, U.W., and D. Jurivich. 1978. Tipping and mating-structure activation induced in Chlamydomonas gametes by flagellar membrane antisera. J. Cell Biol. 79:680-693.
21. Gromley, A., A. Jurczyk, J. Sillibourne, E. Halilovic, M. Mogensen, I. Groisman, M. Blomberg, and S. Doxsey. 2003. A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J. Cell Biol. 161:535-545.
22. Gromley, A., C. Yeaman, J. Rosa, S. Redick, C.T. Chen, S. Mirabelle, M. Guha, J. Sillibourne, and S.J. Doxsey. 2005. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell. 123:75-87.
23. Götz, M., and W.B. Huttner. 2005. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6:777-788.
24. Haubensak, W., A. Attardo, W. Denk, and W.B. Huttner. 2004. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA. 101:3196-3201.
25. Hildebrandt, F., and E. Otto. 2005. Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease? Nat. Rev. Genet. 6:928-940.
26. Hinds, J.W., and T.L. Ruffett. 1971. Cell proliferation in the neural tube: an electron microscopic and Golgi analysis in the mouse cerebral vesicle. Z. Zellforsch. Mikrosk. Anat. 115:226-264.
27. Hirokawa, N., Y. Tanaka, Y. Okada, and S. Takeda. 2006. Nodal flow and the generation of left-right asymmetry. Cell. 125:33-45.
28. Hobbs, D.G. 1980. The origin and distribution of membrane-bound vesicles associated with the brush border of chick intestinal mucosa. J. Anat. 131:635-642.
29. Hollyday, M. 2001. Neurogenesis in the vertebrate neural tube. Int. J. Dev. Neurosci. 19:161-173.
30. Huangfu, D., and K.V. Anderson. 2005. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA. 102:11325-11330.
31. Jones, O.P. 1969. Elimination of midbodies from mitotic erythroblasts and their contribution to fetal blood plasma. J. Natl. Cancer Inst. 42:753-759.
32. Kosodo, Y., K. Röper, W. Haubensak, A.-M. Marzesco, D. Corbeil, and W.B. Huttner. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23:2314-2324.
33. Krull, C.E. 2004. A primer on using in ovo electroporation to analyze gene function. Dev. Dyn. 229:433-439.
34. Lee, A., J.D. Kessler, T.A. Read, C. Kaiser, D. Corbeil, W.B. Huttner, J.E. Johnson, and R.J. Wechsler-Reya. 2005. Isolation of neural stem cells from the postnatal cerebellum. Nat. Neurosci. 8:723-729.
35. Low, S.H., X. Li, M. Miura, N. Kudo, B. Quinones, and T. Weimbs. 2003. Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev. Cell. 4:753-759.
36. Marzesco, A.M., P. Janich, M. Wilsch-Brauninger, V. Dubreuil, K. Langenfeld, D. Corbeil, and W.B. Huttner. 2005. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118:2849-2858.
37. Matheson, J., X. Yu, A.B. Fielding, and G.W. Gould. 2005. Membrane traffic in cytokinesis. Biochem. Soc. Trans. 33:1290-1294.
38. McLean, R., C.J. Laurendi, and R.M. Brown Jr. 1974. The relationship of gamone to the mating reaction in Chlamydomonas moewusii. Proc. Natl. Acad. Sci. USA. 71:2610-2613.
39. Mishima, M., S. Kaitna, and M. Glotzer. 2002. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell. 2:41-54.
40. Momose, T., A. Tonegawa, J. Takeuchi, H. Ogawa, K. Umesono, and K. Yasuda. 1999. Efficient targeting of gene expression in chick embryos by microelectroporation. Dev. Growth Differ. 41:335-344.
41. Mullins, J.M., and J.J. Biesele. 1977. Terminal phase of cytokinesis in D-98s cells. J. Cell Biol. 73:672-684.
42. Mullins, J.M., and J.R. McIntosh. 1982. Isolation and initial characterization of the mammalian midbody. J. Cell Biol. 94:654-661.
43. Muramatsu, T., Y. Mizutani, Y. Ohmori, and J. Okumura. 1997. Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. Biochem. Biophys. Res. Commun. 230:376-380.
44. Nagele, R.G., and H.Y. Lee. 1979. Ultrastructural changes in cells associated with interkinetic nuclear migration in the developing chick neuroepithelium. J. Exp. Zool. 210:89-106.
45. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene. 108:193-199.
46. Oegema, K., M.S. Savoian, T.J. Mitchison, and C.M. Field. 2000. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J. Cell Biol. 150:539-552.
47. Otegui, M.S., K.J. Verbrugghe, and A.R. Skop. 2005. Midbodies and phragmoplasts: analogous structures involved in cytokinesis. Trends Cell Biol. 15:404-413.
48. Pan, J., Q. Wang, and W.J. Snell. 2004. An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell. 6:445-451.
49. Pan, J., Q. Wang, and W.J. Snell. 2005. Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85:452-463.
50. Pazour, G.J., and G.B. Witman. 2003. The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15:105-110.
51. Praetorius, H.A., and K.R. Spring. 2005. A physiological view of the primary cilium. Annu. Rev. Physiol. 67:515-529.
52. Quarmby, L.M., and J.D. Parker. 2005. Cilia and the cell cycle? J. Cell Biol. 169:707-710.
53. Rieder, C.L., C.G. Jensen, and L.C. Jensen. 1979. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line. J. Ultrastruct. Res. 68:173-185.
54. Robbins, E., and N.K. Gonatas. 1964. The ultrastructure of a mammalian cell during the mitotic cycle. J. Cell Biol. 21:429-463.
55. Rosenbaum, J.L., and G.B. Witman. 2002. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3:813-825.
56. Röper, K., D. Corbeil, and W.B. Huttner. 2000. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2:582-592.
57. Scholey, J.M., and K.V. Anderson. 2006. Intraflagellar transport and cilium-based signaling. Cell. 125:439-442.
58. Schweitzer, J.K., and C. D'Souza-Schorey. 2004. Finishing the job: cytoskeletal and membrane events bring cytokinesis to an end. Exp. Cell Res. 295:1-8.
59. Skop, A.R., H. Liu, J. Yates III, B.J. Meyer, and R. Heald. 2004. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science. 305:61-66.
60. Snell, W.J. 1976. Mating in Chlamydomonas: a system for the study of specific cell adhesion. I. Ultrastructural and electrophoretic analyses of flagellar surface components involved in adhesion. J. Cell Biol. 68:48-69.
61. Snell, W.J., J. Pan, and Q. Wang. 2004. Cilia and flagella revealed: from flagellar assembly in Chlamydomonas to human obesity disorders. Cell. 117:693-697.
62. Sorokin, S.P. 1968. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3:207-230.
63. Steegmaier, M., E. Borges, J. Berger, H. Schwarz, and D. Vestweber. 1997. The E-selectin-ligand ESL-1 is located in the Golgi as well as on microvilli on the cell surface. J. Cell Sci. 110:687-694.
64. Stoorvogel, W., M.J. Kleijmeer, H.J. Geuze, and G. Raposo. 2002. The biogenesis and functions of exosomes. Traffic. 3:321-330.
65. Tanaka, Y., Y. Okada, and N. Hirokawa. 2005. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature. 435:172-177.
66. Théry, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2:569-579.
67. Weigmann, A., D. Corbeil, A. Hellwig, and W.B. Huttner. 1997. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc. Natl. Acad. Sci. USA. 94:12425-12430.
68. Yin, A.H., S. Miraglia, E.D. Zanjani, G. Almeida-Porada, M. Ogawa, A.G. Leary, J. Olweus, J. Kearney, and D.W. Buck. 1997. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 90:5002-5012.