Non-canonical features of the Golgi apparatus in bipolar epithelial neural stem cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Taverna, Elena ^a   Mora Bermúdez, Felipe ^a   Strzyz, Paulina J ^a   Florio, Marta ^a   Icha, Jaroslav ^a   Haffner, Christiane ^a   Norden, Caren ^a   Wilsch Braüninger, Michaela ^a   Huttner, Wieland B ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDE;

ANIMAL; CELL MEMBRANE; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; GENE EXPRESSION; GOLGI COMPLEX; METABOLISM; MITOSIS; MOUSE; NEURAL STEM CELL; PROTEIN TRANSPORT; REPORTER GENE; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALS; CELL MEMBRANE; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; GENE EXPRESSION; GENES, REPORTER; GOLGI APPARATUS; MICE; MICE, TRANSGENIC; MITOSIS; NEURAL STEM CELLS; POLYSACCHARIDES; PROTEIN TRANSPORT;

EID: 84958267539     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21206     Document Type: Article

References (81)

1. Götz, M., Huttner, W. B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788 (2005).
2. Taverna, E., Götz, M., Huttner, W. B. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu. Rev. Cell Dev. Biol. 30, 465-502 (2014).
3. Paridaen, J. T., Huttner, W. B. Neurogenesis during development of the vertebrate central nervous system. EMBO reports 15, 351-64 (2014).
4. Taverna, E., Huttner, W. B. Neural progenitor nuclei IN Motion. Neuron 67, 906-914 (2010).
5. Lee, H. O., Norden, C. Mechanisms controlling arrangements and movements of nuclei in pseudostratified epithelia. Trends Cell Biol 23, 141-50 (2013).
6. Götz, M., Barde, Y. A. Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46, 369-72 (2005).
7. Haubensak, W., Attardo, A., Denk, W., Huttner, W. B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101, 3196-3201 (2004).
8. Miyata, T. et al. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145 (2004).
9. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144 (2004).
10. Kowalczyk, T. et al. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19, 2439-2450 (2009).
11. Mostov, K. E., Verges, M., Altschuler, Y. Membrane traffic in polarized epithelial cells. Curr Opin Cell Biol. 12, 483-490 (2000).
12. Bacallao, R. et al. The Subcellular Organization of Madin-Darby Canine Kidney Cells during the Formation of a Polarized Epithelium. JCB 109, 2817-2832 (1989).
13. Sutterlin, C., Colanzi, A. The Golgi and the centrosome: building a functional partnership. J Cell Biol 188, 621-8 (2010).
14. Yadav, S., Puri, S., Linstedt, A. D. A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol Biol Cell 20, 1728-36 (2009).
15. Colanzi, A., Suetterlin, C., Malhotra, V. Cell-cycle-specific Golgi fragmentation: how and why? Curr Opin Cell Biol 15, 462-7 (2003).
16. Sutterlin, C., Hsu, P., Mallabiabarrena, A., Malhotra, V. Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell 109, 359-69 (2002).
17. Hurtado, L. et al. Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. J Cell Biol 193, 917-33 (2011).
18. Nolte, C. et al. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33, 72-86 (2001).
19. Pinto, L. et al. Prospective isolation of functionally distinct radial glial subtypes-lineage and transcriptome analysis. Mol Cell Neurosci 38, 15-42 (2008).
20. Beckervordersandforth, R. et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7, 744-58 (2010).
21. Veenendaal, T. et al. GRASP65 controls the cis Golgi integrity in vivo. Biol Open 3, 431-43 (2014).
22. Vinke, F. P., Grieve, A. G., Rabouille, C. The multiple facets of the Golgi reassembly stacking proteins. Biochem J 433, 423-33 (2011).
23. Linstedt, A. D., Hauri, H. P. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol Biol Cell 4, 679-93 (1993).
24. Denk, W., Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2, e329 (2004).
25. Helmstaedter, M., Briggman, K. L., Denk, W. 3D structural imaging of the brain with photons and electrons. Curr Opin Neurobiol 18, 633-41 (2008).
26. Mora-Bermudez, F., Matsuzaki, F., Huttner, W. B. Specific polar subpopulations of astral microtubules control spindle orientation and symmetric neural stem cell division. eLife 3 (2014).
27. Levine, T. P., Misteli, T., Rabouille, C., Warren, G. Mitotic disassembly and reassembly of the Golgi apparatus. Cold Spring Harb Symp Quant Biol 60, 549-57 (1995).
28. Lucocq, J. M., Berger, E. G., Warren, G. Mitotic Golgi Fragments in HeLa Cells and Their Role in the Reassembly Pathway. J. Cell Biol. 109, 463-474 (1989).
29. Warren, G., Malhotra, V. The organisation of the Golgi apparatus. Curr Opin Cell Biol 10, 493-8 (1998).
30. Wilsch-Braüninger, M., Peters, J., Paridaen, J. T. M. L., Huttner, W. B. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139, 95-105 (2012).
31. Paridaen, J. T., Wilsch-Brauninger, M., Huttner, W. B. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155, 333-44 (2013).
32. Leung, L., Klopper, A. V., Grill, S. W., Harris, W. A., Norden, C. Apical migration of nuclei during G2 is a prerequisite for all nuclear motion in zebrafish neuroepithelia. Development 138, 5003-13 (2011).
33. Thyberg, J., Moskalewski, S. Microtubules and the organization of the Golgi complex. Exp. Cell Res. 159, 1-16 (1985).
34. Kwon, G. S., Hadjantonakis, A. K. Eomes::GFP-a tool for live imaging cells of the trophoblast, primitive streak, and telencephalon in the mouse embryo. Genesis 45, 208-17 (2007).
35. Schenk, J., Wilsch-Brauninger, M., Calegari, F., Huttner, W. B. Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci USA 106, 16487-92 (2009).
36. Shima, D. T., Haldar, K., Pepperkok, R., Watson, R., Warren, G. Partitioning of the Golgi apparatus during mitosis in living HeLa cells. J Cell Biol 137, 1211-28 (1997).
37. Shima, D. T., Cabrera-Poch, N., Pepperkok, R., Warren, G. An ordered inheritance strategy for the Golgi apparatus: visualization of mitotic disassembly reveals a role for the mitotic spindle. J Cell Biol 141, 955-66 (1998).
38. Rabouille, C., Jokitalo, E. Golgi apparatus partitioning during cell division. Mol Membr Biol 20, 117-27 (2003).
39. Thyberg, J., Moskalewski, S. Reorganization of the Golgi complex in association with mitosis: redistribution of mannosidase II to the endoplasmic reticulum and effects of brefeldin A. J Submicrosc Cytol Pathol 24, 495-508 (1992).
40. Moskalewski, S., Thyberg, J. Synchronized shift in localization of the Golgi complex and the microtubule organizing center in the terminal phase of cytokinesis. J Submicrosc Cytol Pathol 24, 359-70 (1992).
41. Zaal, K. J. et al. Golgi membranes are absorbed into and reemerge from the ER during mitosis. Cell 99, 589-601 (1999).
42. Ettinger, A. W. et al. Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat Comm 2, 503 (2011).
43. Park, E., Rapoport, T. A. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 41, 21-40 (2012).
44. Deshaies, R. J., Schekman, R. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J Cell Biol 105, 633-45 (1987).
45. Kaiser, C., Schekman, R. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61, 723-733 (1990).
46. Rabouille, C., Malhotra, V., Nickel, W. Diversity in unconventional protein secretion. J Cell Sci 125, 5251-5 (2012).
47. Kinseth, M. A. et al. The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 130, 524-34 (2007).
48. Schafer, T. et al. Unconventional secretion of fibroblast growth factor 2 is mediated by direct translocation across the plasma membrane of mammalian cells. J Biol Chem 279, 6244-51 (2004).
49. Nickel, W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 270, 2109-19 (2003).
50. Aebi, M., Bernasconi, R., Clerc, S., Molinari, M. N-glycan structures: recognition and processing in the ER. Trends Biochem Sci 35, 74-82 (2010).
51. Florio, M. et al. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347, 1465-1470 (2015).
52. Aaku-Saraste, E., Hellwig, A., Huttner, W. B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180, 664-679 (1996).
53. Lee, I. et al. Membrane adhesion dictates Golgi stacking and cisternal morphology. Proc Natl Acad Sci USA 111, 1849-54 (2014).
54. Guet, D. et al. Mechanical role of actin dynamics in the rheology of the Golgi complex and in Golgi-associated trafficking events. Curr Biol 24, 1700-11 (2014).
55. Altan-Bonnet, N. et al. Golgi inheritance in mammalian cells is mediated through endoplasmic reticulum export activities. Mol Biol Cell 17, 990-1005 (2006).
56. Miserey-Lenkei, S. et al. A role for the Rab6A' GTPase in the inactivation of the Mad2-spindle checkpoint. EMBO J 25, 278-89 (2006).
57. Vallee, R. B., Varma, D., Dujardin, D. L. ZW10 function in mitotic checkpoint control, dynein targeting and membrane trafficking: is dynein the unifying theme? Cell Cycle 5, 2447-51 (2006).
58. Zhou, Y. et al. The mammalian Golgi regulates numb signaling in asymmetric cell division by releasing ACBD3 during mitosis. Cell 129, 163-78 (2007).
59. Horton, A. C., Ehlers, M. D. Neuronal polarity and trafficking. Neuron 40, 277-95 (2003).
60. Horton, A. C., Ehlers, M. D. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23, 6188-99 (2003).
61. Horton, A. C., Ehlers, M. D. Secretory trafficking in neuronal dendrites. Nat Cell Biol 6, 585-91 (2004).
62. Bloom, O. E., Morgan, J. R. Membrane trafficking events underlying axon repair, growth, and regeneration. Mol Cell Neurosci 48, 339-48 (2011).
63. Holcomb, P. S., Deerinck, T. J., Ellisman, M. H., Spirou, G. A. Construction of a polarized neuron. J Physiol 591, 3145-50 (2013).
64. Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011).
65. Grieve, A. G., Rabouille, C. Golgi bypass: skirting around the heart of classical secretion. Cold Spring Harb Perspect Biol 3, a005298 (2011).
66. Schotman, H., Karhinen, L., Rabouille, C. Integrins mediate their unconventional, mechanical-stress-induced secretion via RhoA and PINCH in Drosophila. J Cell Sci 122, 2662-72 (2009).
67. Schotman, H., Karhinen, L., Rabouille, C. dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell 14, 171-82 (2008).
68. Bielas, S., Higginbotham, H., Koizumi, H., Tanaka, T., Gleeson, J. G. Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu Rev Cell Dev Biol 20, 593-618 (2004).
69. Hatten, M. E. Central nervous system neuronal migration. Ann Rev Neurosci 22, 511-39 (1999).
70. Nadarajah, B., Parnavelas, J. G. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3, 423-32 (2002).
71. Attardo, A., Calegari, F., Haubensak, W., Wilsch-Braüninger, M., Huttner, W. B. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS ONE 3, e2388 (2008).
72. Taverna, E., Haffner, C., Pepperkok, R., Huttner, W. B. A new approach to manipulate the fate of single neural stem cells in tissue. Nat. Neurosci. 15, 329-337 (2012).
73. Cardona, A., Tomancak, P. Current challenges in open-source bioimage informatics. Nat Methods 9, 661-5 (2012).
74. Mora-Bermudez, F., Ellenberg, J. Measuring structural dynamics of chromosomes in living cells by fluorescence microscopy. Methods 41, 158-67 (2007).
75. Norden, C., Young, S., Link, B. A., Harris, W. A. Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138, 1195-208 (2009).
76. Weber, I. P. et al. Mitotic position and morphology of committed precursor cells in the zebrafish retina adapt to architectural changes upon tissue maturation. Cell Rep 7, 386-97 (2014).
77. Strzyz, P. J. et al. Interkinetic nuclear migration is centrosome independent and ensures apical cell division to maintain tissue integrity. Dev Cell 32, 203-19 (2015).
78. Insinna, C., Baye, L. M., Amsterdam, A., Besharse, J. C., Link, B. A. Analysis of a zebrafish dync1h1 mutant reveals multiple functions for cytoplasmic dynein 1 during retinal photoreceptor development. Neural Dev 5, 12 (2010).
79. Kwan, K. M. et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236, 3088-99 (2007).
80. Bussow, K. et al. Structural genomics of human proteins-target selection and generation of a public catalogue of expression clones. Microb Cell Fact 4, 21 (2005).
81. Reboutier, D. et al. Aurora A is involved in central spindle assembly through phosphorylation of Ser 19 in P150Glued. J Cell Biol 201, 65-79 (2013).