The endoplasmic reticulum is partitioned asymmetrically during mitosis before cell fate selection in proneuronal cells in the early Drosophila embryo

Molecular Biology of the Cell

Volumn 28, Issue 11, 2017, Pages 1530-1538

  Eritano, Anthony S ^a   Altamirano, Arturo ^a   Beyeler, Sarah ^a   Gaytan, Norma ^a   Velasquez, Mark ^a   Riggs, Blake ^a  

^a SAN FRANCISCO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; JAGUNAL PROTEIN; MEMBRANE PROTEIN; PROTEIN; PROTEIN KINASE C; RED FLUORESCENT PROTEIN; RETICULON 1 PROTEIN; RNA; TUBULIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DROSOPHILA PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; ASYMMETRIC CELL DIVISION; BLASTODERM; CELL FATE; CELL POPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME INHIBITION; EPITHELIUM CELL; GASTRULATION; METAPHASE; MITOSIS; NERVE CELL; NEUROBLAST; NONHUMAN; POPULATION; PRIORITY JOURNAL; PROMETAPHASE; RNA INTERFERENCE; SPINDLE CELL; ANIMAL; CELL DIFFERENTIATION; CELL DIVISION; CELL POLARITY; EMBRYOLOGY; METABOLISM; PHYSIOLOGY; SPINDLE APPARATUS; STEM CELL;

ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL POLARITY; DROSOPHILA; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; MITOSIS; NEURONS; SPINDLE APPARATUS; STEM CELLS;

EID: 85020092288     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-09-0690     Document Type: Article

References (52)

1. Ashburner M (1989). Drosophila: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
2. Bardin AJ, Le Borgne R, Schweisguth F (2004). Asymmetric localization and function of cell-fate determinants: a fy's view. Curr Opin Neurobiol 14, 6-14.
3. Bergman ZJ, Mclaurin JD, Eritano AS, Johnson BM, Sims AQ, Riggs B (2015). Spatial reorganization of the endoplasmic reticulum during mitosis relies on mitotic kinase cyclin A in the early Drosophila embryo. PLoS One 10, e0117859.
4. Bobinnec Y, Marcaillou C, Morin X, Debec A (2003). Dynamics of the endo-plasmic reticulum during early development of Drosophila melanogas-ter. Cell Motil Cytoskeleton 54, 217-225.
5. Boztug K, Järvinen PM, Salzer E, Racek T, Mönch S, Garncarz W, Gertz EM, Schäffer AA, Antonopoulos A, Haslam SM, et al. (2014). JAGN1 defciency causes aberrant myeloid cell homeostasis and congenital neutropenia. Nat Genet 46, 1021-1027.
6. Campos-Ortega JA, Hartenstein V (1997). The Embryonic Development of Drosophila melanogaster, New York: Springer.
7. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, et al. (2006). CellProfler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7, R100.
8. Chang P, Torres J, Lewis RA, Mowry KL, Houliston E, King ML (2004). Localization of RNAs to the mitochondrial cloud in Xenopus oocytes through entrapment and association with endoplasmic reticulum. Mol Biol Cell 15, 4669-4681.
9. Cosson P, Lefkir Y, Demolliere C, Letourneur F (1998). New COP1-binding motifs involved in ER retrieval. EMBO J 17, 6863-6870.
10. Doe CQ (1992). Molecular markers for identifed neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 116, 855-863.
11. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP (1991). The prospero gene specifes cell fates in the Drosophila central nervous system. Cell 65, 451-464.
12. Estrada P, Kim J, Coleman J, Walker L, Dunn B, Takizawa P, Novick P, Ferro-Novick S (2003). Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J Cell Biol 163, 1255-1266.
13. Foe VE (1989). Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107, 1-22.
14. Foe VE, Alberts BM (1983). Studies of nuclear and cytoplasmic behaviour during the fve mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61, 31-70.
15. Foe VE, Odell GM, Edgar BA (1993). Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In: The Development of Drosophila melanogaster, ed. M Bate and A Martinez Arias, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 149-300.
16. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421.
17. Jan YN, Jan LY (2001). Polarity in cell division. Cell 100, 599-602.
18. John NW, McCloy RF (2014). Navigating and visualizing three-dimensional data sets. Br J Radiol 77, Spec No 2S108S113.
19. Knoblich JA (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
20. Kraut R, Chia W, Jan LY, Jan YN, Knoblich JA (1996). Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383, 50-55.
21. Kuchinke U, Grawe F, Knust E (1998). Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka. Curr Biol 8, 1357-1365.
22. Lechler T, Fuchs E (2005). Asymmetric cell divisions promote stratifcation and differentiation of mammalian skin. Nature 437, 275-280.
23. Lee S, Cooley L (2007). Jagunal is required for reorganizing the endoplas-mic reticulum during Drosophila oogenesis. J Cell Biol 176, 941-952.
24. Lu L, Ladinsky MS, Kirchhausen T (2009). Cisternal organization of the endo-plasmic reticulum during mitosis. Mol Biol Cell 20, 3471-3480.
25. Lu MS, Johnston CA (2013). Molecular pathways regulating mitotic spindle orientation in animal cells. Development 140, 1843-1856.
26. McCullough S, Lucocq J (2005). Endoplasmic reticulum positioning and partitioning in mitotic HeLa cells. J Anat 206, 415-425.
27. Mehlmann LM, Terasaki M, Jaffe LA, Kline D (1995). Reorganization of the endoplasmic reticulum during meiotic maturation of the mouse oocyte. Dev Biol 170, 607-615.
28. Morin X, Daneman R, Zavortink M, Chia W (2001). A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci USA 98, 15050-15055.
29. Nakamura Y, Makabe KW, Nishida H (2005). POPK-1/Sad-1 kinase is required for the proper translocation of maternal mRNAs and putative germ plasm at the posterior pole of the ascidian embryo. Development 132, 4731-4742.
30. Nishikata T, Hibino T, Nishida H (1999). The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev Biol 209, 72-85.
31. Parry H (2005). Microdomains bounded by endoplasmic reticulum segregate cell cycle calcium transients in syncytial Drosophila embryos. J Cell Biol 171, 47-59.
32. Patalano S, Prulière G, Prodon F, Paix A, Dru P, Sardet C, Chenevert J (2006). The aPKC-PAR-6-PAR-3 cell polarity complex localizes to the centrosome attracting body, a macroscopic cortical structure responsible for asymmetric divisions in the early ascidian embryo. J Cell Sci 119, 1592-1603.
33. Petronczki M, Knoblich JA (2001). DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila. Nat Cell Biol 3, 43-49.
34. Poteryaev D, Squirrell JM, Campbell JM, White JG, Spang A (2005). In-volvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Mol Biol Cell 16, 2139-2153.
35. Prodon F, Chenevert J, Hébras C, Dumollard R, Faure E, Gonzalez-Garcia J, Nishida H, Sardet C, McDougall A (2010). Dual mechanism controls asymmetric spindle position in ascidian germ cell precursors. Development 137, 2011-2021.
36. Riggs B, Fasulo B, Royou A, Mische S, Cao J, Hays TS, Sullivan W (2007). The concentration of Nuf, a Rab11 effector, at the microtubule-organiz-ing center is cell cycle regulated, dynein-dependent, and coincides with furrow formation. Mol Biol Cell 18, 3313-3322.
37. Roegiers F, Jan YN (2004). Asymmetric cell division. Curr Opin Cell Biol 16, 195-205.
38. Rolls MM, Albertson R, Shih HP, Lee CY, Doe CQ (2003). Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. J Cell Biol 163, 1089-1098.
39. Sardet C, Paix A, Prodon F, Dru P, Chenevert J (2007). From oocyte to 16-cell stage: cytoplasmic and cortical reorganizations that pattern the ascidian embryo. Dev Dyn 236, 1716-1731.
40. Sardet C, Speksnijder J, Terasaki M, Chang P (1992). Polarity of the ascidian egg cortex before fertilization. Development 115, 221-237.
41. Schejter ED, Wieschaus E (1993). Functional elements of the cytoskeleton in the early Drosophila embryo. Annu Rev Cell Biol 9, 67-99.
42. Siegrist SE, Doe CQ (2006). Extrinsic cues orient the cell division axis in Drosophila embryonic neuroblasts. Development 133, 529-536.
43. Smyth JT, Beg AM, Wu S, Putney JW Jr, Rusan NM (2012). Phosphoregula-tion of STIM1 leads to exclusion of the endoplasmic reticulum from the mitotic spindle. Curr Biol 22, 1487-1493.
44. Smyth JT, Schoborg TA, Bergman ZJ, Riggs B, Rusan NM (2015). Proper symmetric and asymmetric endoplasmic reticulum partitioning requires astral microtubules. Open Biol 5, 150067.
45. Technau GM, Berger C, Urbach R (2006). Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev Dyn 235, 861-869.
46. Terasaki M, Chen LB, Fujiwara K (1986). Microtubules and the endoplas-mic reticulum are highly interdependent structures. J Cell Biol 103, 1557-1568.
47. Terasaki M, Runft LL, Hand AR (2001). Changes in organization of the en-doplasmic reticulum during Xenopus oocyte maturation and activation. Mol Biol Cell 12, 1103-1116.
48. Terasaki M, Song J, Wong JR, Weiss MJ, Chen LB (1984). Localization of endoplasmic reticulum in living and glutaraldehyde-fxed cells with fuorescent dyes. Cell 38, 101-108.
49. Urbach R, Schnabel R, Technau GM (2003). The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130, 3589-3606.
50. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006). A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573-586.
51. Wakefeld S, Tear G (2006). The Drosophila reticulon, Rtnl-1, has multiple differentially expressed isoforms that are associated with a sub-compartment of the endoplasmic reticulum. Cell Mol Life Sci 63, 2027-2038.
52. Williams SE, Beronja S, Pasolli HA, Fuchs E (2011). Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 470, 353-358.