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Microtubules are necessary for proper Reticulon localization during mitosis


Autoři: Ulises Diaz aff001;  Zane J. Bergman aff001;  Brittany M. Johnson aff001;  Alia R. Edington aff001;  Matthew A. de Cruz aff001;  Wallace F. Marshall aff002;  Blake Riggs aff001
Působiště autorů: Department of Biology, San Francisco State University, San Francisco, California, United States of America aff001;  Department of Biochemistry & Biophysics, UCSF Mission Bay, San Francisco, California, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226327

Souhrn

During mitosis, the structure of the Endoplasmic Reticulum (ER) displays a dramatic reorganization and remodeling, however, the mechanism driving these changes is poorly understood. Hairpin-containing ER transmembrane proteins that stabilize ER tubules have been identified as possible factors to promote these drastic changes in ER morphology. Recently, the Reticulon and REEP family of ER shaping proteins have been shown to heavily influence ER morphology by driving the formation of ER tubules, which are known for their close proximity with microtubules. Here, we examine the role of microtubules and other cytoskeletal factors in the dynamics of a Drosophila Reticulon, Reticulon-like 1 (Rtnl1), localization to spindle poles during mitosis in the early embryo. At prometaphase, Rtnl1 is enriched to spindle poles just prior to the ER retention motif KDEL, suggesting a possible recruitment role for Rtnl1 in the bulk localization of ER to spindle poles. Using image analysis-based methods and precise temporal injections of cytoskeletal inhibitors in the early syncytial Drosophila embryo, we show that microtubules are necessary for proper Rtnl1 localization to spindles during mitosis. Lastly, we show that astral microtubules, not microfilaments, are necessary for proper Rtnl1 localization to spindle poles, and is largely independent of the minus-end directed motor protein dynein. This work highlights the role of the microtubule cytoskeleton in Rtnl1 localization to spindles during mitosis and sheds light on a pathway towards inheritance of this major organelle.

Klíčová slova:

Cytoplasm – Drosophila melanogaster – Dyneins – Embryos – Endoplasmic reticulum – Metaphase – Microtubules – Mitosis


Zdroje

1. Lancaster OM, Baum B. Shaping up to divide: coordinating actin and microtubule cytoskeletal remodelling during mitosis. In Seminars in cell & developmental biology 2014 Oct 1 (Vol. 34, pp. 109–115). Academic Press. doi: 10.1016/j.semcdb.2014.02.015 24607328

2. Walczak CE, Cai S, Khodjakov A. Mechanisms of chromosome behaviour during mitosis. Nature reviews Molecular cell biology. 2010 Feb;11(2):91. doi: 10.1038/nrm2832 20068571

3. McIntosh JR, Grishchuk EL, West RR. Chromosome-microtubule interactions during mitosis. Annual review of cell and developmental biology. 2002 Nov;18(1):193–219. doi: 10.1146/annurev.cellbio.18.032002.132412 12142285

4. Persico A, Cervigni RI, Barretta ML, Colanzi A. Mitotic inheritance of the Golgi complex. FEBS letters. 2009 Dec 3;583(23):3857–62. doi: 10.1016/j.febslet.2009.10.077 19879264

5. Altan-Bonnet N, Sougrat R, Lippincott-Schwartz J. Molecular basis for Golgi maintenance and biogenesis. Current opinion in cell biology. 2004 Aug 1;16(4):364–72. doi: 10.1016/j.ceb.2004.06.011 15261668

6. McCullough S, Lucocq J. Endoplasmic reticulum positioning and partitioning in mitotic HeLa cells. Journal of Anatomy. 2005 May;206(5):415–25. doi: 10.1111/j.1469-7580.2005.00407.x 15857362

7. Lu L, Ladinsky MS, Kirchhausen T. Cisternal organization of the endoplasmic reticulum during mitosis. Molecular biology of the cell. 2009 Aug 1;20(15):3471–80. doi: 10.1091/mbc.E09-04-0327 19494040

8. Puhka M, Vihinen H, Joensuu M, Jokitalo E. Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. The Journal of cell biology. 2007 Dec 3;179(5):895–909. doi: 10.1083/jcb.200705112 18056408

9. Puhka M, Joensuu M, Vihinen H, Belevich I, Jokitalo E. Progressive sheet-to-tubule transformation is a general mechanism for endoplasmic reticulum partitioning in dividing mammalian cells. Molecular biology of the cell. 2012 Jul 1;23(13):2424–32. doi: 10.1091/mbc.E10-12-0950 22573885

10. Bisel B, Wang Y, Wei JH, Xiang Y, Tang D, Miron-Mendoza M, Yoshimura SI, Nakamura N, Seemann J. ERK regulates Golgi and centrosome orientation towards the leading edge through GRASP65. The Journal of cell biology. 2008 Sep 8;182(5):837–43. doi: 10.1083/jcb.200805045 18762583

11. Bergman ZJ, Mclaurin JD, Eritano AS, Johnson BM, Sims AQ, Riggs B. Spatial reorganization of the endoplasmic reticulum during mitosis relies on mitotic kinase cyclin A in the early Drosophila embryo. PloS one. 2015 Feb 17;10(2):e0117859. doi: 10.1371/journal.pone.0117859 25689737

12. Champion L, Linder MI, Kutay U. Cellular reorganization during mitotic entry. Trends in cell biology. 2017 Jan 1;27(1):26–41. doi: 10.1016/j.tcb.2016.07.004 27528558

13. Wittmann T, Hyman A, Desai A. The spindle: a dynamic assembly of microtubules and motors. Nature cell biology. 2001 Jan;3(1):E28. doi: 10.1038/35050669 11146647

14. O’Connell CB, Khodjakov AL. Cooperative mechanisms of mitotic spindle formation. Journal of cell science. 2007 May 15;120(10):1717–22. doi: 10.1242/jcs.03442 17502482

15. Terasaki M, Chen LB, Fujiwara K. Microtubules and the endoplasmic reticulum are highly interdependent structures. The Journal of cell biology. 1986 Oct 1;103(4):1557–68. doi: 10.1083/jcb.103.4.1557 3533956

16. Waterman-Storer CM, Salmon ED. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Current Biology. 1998 Jul 2;8(14):798–807. doi: 10.1016/s0960-9822(98)70321-5 9663388

17. Bobinnec Y, Marcaillou C, Morin X, Debec A. Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell motility and the cytoskeleton. 2003 Mar;54(3):217–25. doi: 10.1002/cm.10094 12589680

18. Anderson DJ, Hetzer MW. Shaping the endoplasmic reticulum into the nuclear envelope. Journal of cell science. 2008 Jan 15;121(2):137–42. doi: 10.1242/jcs.005777 18187447

19. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 2006 Feb 10;124(3):573–86. doi: 10.1016/j.cell.2005.11.047 16469703

20. Shibata Y, Voss C, Rist JM, Hu J, Rapoport TA, Prinz WA, Voeltz GK. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. Journal of Biological Chemistry. 2008 Jul 4;283(27):18892–904. doi: 10.1074/jbc.M800986200 18442980

21. Hu J, Shibata Y, Voss C, Shemesh T, Li Z, Coughlin M, Kozlov MM, Rapoport TA, Prinz WA. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science. 2008 Feb 29;319(5867):1247–50. doi: 10.1126/science.1153634 18309084

22. Sanderson CM, Connell JW, Edwards TL, Bright NA, Duley S, Thompson A, Luzio JP, Reid E. Spastin and atlastin, two proteins mutated in autosomal-dominant hereditary spastic paraplegia, are binding partners. Human molecular genetics. 2005 Dec 8;15(2):307–18. doi: 10.1093/hmg/ddi447 16339213

23. Yang YS, Strittmatter SM. The reticulons: a family of proteins with diverse functions. Genome biology. 2007 Dec;8(12):234. doi: 10.1186/gb-2007-8-12-234 18177508

24. Yalçın B, Zhao L, Stofanko M, O’Sullivan NC, Kang ZH, Roost A, Thomas MR, Zaessinger S, Blard O, Patto AL, Sohail A. Modeling of axonal endoplasmic reticulum network by spastic paraplegia proteins. Elife. 2017 Jul 25;6:e23882. doi: 10.7554/eLife.23882 28742022

25. Kumar D, Golchoubian B, Belevich I, Jokitalo E, Schlaitz AL. REEP3 and REEP4 determine the tubular morphology of the endoplasmic reticulum during mitosis. Molecular biology of the cell. 2019 Jun 1;30(12):1377–89. doi: 10.1091/mbc.E18-11-0698 30995177

26. Schlaitz AL. Microtubules as key coordinators of nuclear envelope and endoplasmic reticulum dynamics during mitosis. Bioessays. 2014 Jul;36(7):665–71. doi: 10.1002/bies.201400022 24848719

27. Tram U, Riggs B, Sullivan W. Cleavage and gastrulation in Drosophila embryos. e LS. 2001 May 30. doi: 10.1038/npg.els.0001071

28. Sharp DJ. Rogers GC, Scholey JM. Microtubule motors in mitosis. Nature. 2000; 407:41–7. doi: 10.1038/35024000 10993066

29. Brust-Mascher I, Scholey JM. Microtubule flux and sliding in mitotic spindles of Drosophila embryos. Molecular biology of the cell. 2002 Nov 1;13(11):3967–75. doi: 10.1091/mbc.02-05-0069 12429839

30. Fenton B, Glover DM. A conserved mitotic kinase active at late anaphase—telophase in syncitial Drosophila embryos. Nature. 1993 Jun;363(6430):637. doi: 10.1038/363637a0 8510757

31. Frescas D, Mavrakis M, Lorenz H, DeLotto R, Lippincott-Schwartz J. The secretory membrane system in the Drosophila syncitial blastoderm embryo exists as functionally compartmentalized units around individual nuclei. J Cell Biol. 2006 Apr 24;173(2):219–30. doi: 10.1083/jcb.200601156 16636144

32. Campos-Ortega JA, Hartenstein V. The embryonic development of Drosophila melanogaster. Springer Science & Business Media; 2013 Nov 11 doi: 10.1007/978-3-662-22489-2_2

33. Riggs B, Fasulo B, Royou A, Mische S, Cao J, Hays TS, Sullivan W. The Concentration of Nuf, a Rab11 Effector, at the Microtubule-organizing Center Is Cell Cycle–regulated, Dynein-dependent, and Coincides with Furrow Formation. Molecular biology of the cell. 2007 Sep;18(9):3313–22. doi: 10.1091/mbc.E07-02-0146 17581858

34. Raff JW, Glover DM. Centrosomes, and not nuclei, initiate pole cell formation in Drosophila embryos. Cell. 1989 May 19;57(4):611–9. doi: 10.1016/0092-8674(89)90130-x 2497990

35. Morin X, Daneman R, Zavortink M, Chia W. A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proceedings of the National Academy of Sciences. 2001 Dec 18;98(26):15050–5. doi: 10.1073/pnas.261408198 11742088

36. Klopfenstein DR, Kappeler F, Hauri HP. A novel direct interaction of endoplasmic reticulum with microtubules. The EMBO journal. 1998 Nov 2;17(21):6168–77. doi: 10.1093/emboj/17.21.6168 9799226

37. Cao J, Crest J, Fasulo B, Sullivan W. Cortical actin dynamics facilitate early-stage centrosome separation. Current Biology. 2010 Apr 27;20(8):770–6. doi: 10.1016/j.cub.2010.02.060 20409712

38. Lantz VA, Miller KG. A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein–170, in neurons and at the posterior pole of Drosophila embryos. The Journal of cell biology. 1998 Feb 23;140(4):897–910. doi: 10.1083/jcb.140.4.897 9472041

39. Crest J, Concha-Moore K, Sullivan W. RhoGEF and positioning of rappaport-like furrows in the early Drosophila embryo. Current Biology. 2012 Nov 6;22(21):2037–41. doi: 10.1016/j.cub.2012.08.046 23022066

40. Poteryaev D, Squirrell JM, Campbell JM, White JG, Spang A. Involvement of the actin cytoskeleton and homotypic membrane fusion in ER dynamics in Caenorhabditis elegans. Molecular biology of the cell. 2005 May;16(5):2139–53. doi: 10.1091/mbc.E04-08-0726 15716356

41. Mermall V, McNally JG, Miller KG. Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos. Nature. 1994 Jun;369(6481):560. doi: 10.1038/369560a0 8202156

42. Papoulas O, Hays TS, Sisson JC. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nature cell biology. 2005 Jun;7(6):612. doi: 10.1038/ncb1264 15908943

43. Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, Gould GW, Sullivan W. Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol. 2003 Oct 13;163(1):143–54. doi: 10.1083/jcb.200305115 14530382

44. Field CM, Alberts BM. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. The Journal of cell biology. 1995 Oct 1;131(1):165–78. doi: 10.1083/jcb.131.1.165 7559773

45. González C, Tavosanis G, Mollinari C. Centrosomes and microtubule organisation during Drosophila development. Journal of Cell Science. 1998 Sep 15;111(18):2697–706.

46. Megraw TL, Li K, Kao LR, Kaufman TC. The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development. 1999 Jul 1;126(13):2829–39. 10357928

47. Smurnyy Y, Toms AV, Hickson GR, Eck MJ, Eggert US. Binucleine 2, an isoform-specific inhibitor of Drosophila Aurora B kinase, provides insights into the mechanism of cytokinesis. ACS chemical biology. 2010 Aug 30;5(11):1015–20. doi: 10.1021/cb1001685 20804174

48. Giet R, Glover DM. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. The Journal of cell biology. 2001 Feb 19;152(4):669–82. doi: 10.1083/jcb.152.4.669 11266459

49. Resnick TD, Satinover DL, MacIsaac F, Stukenberg PT, Earnshaw WC, Orr-Weaver TL, Carmena M. INCENP and Aurora B promote meiotic sister chromatid cohesion through localization of the Shugoshin MEI-S332 in Drosophila. Developmental cell. 2006 Jul 1;11(1):57–68. doi: 10.1016/j.devcel.2006.04.021 16824953

50. Kallio MJ, McCleland ML, Stukenberg PT, Gorbsky GJ. Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Current Biology. 2002 Jun 4;12(11):900–5. doi: 10.1016/s0960-9822(02)00887-4 12062053

51. Schumacher JM, Golden A, Donovan PJ. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. The Journal of cell biology. 1998 Dec 14;143(6):1635–46 doi: 10.1083/jcb.143.6.1635 9852156

52. Kwon M, Scholey JM. Spindle mechanics and dynamics during mitosis in Drosophila. Trends in cell biology. 2004 Apr 1;14(4):194–205. doi: 10.1016/j.tcb.2004.03.003 15066637

53. Glover DM, Leibowitz MH, McLean DA, Parry H. Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell. 1995 Apr 7;81(1):95–105. doi: 10.1016/0092-8674(95)90374-7 7720077

54. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol. 2003 Apr 28;161(2):267–80. doi: 10.1083/jcb.200208091 12719470

55. Bastos RN, Gandhi SR, Baron RD, Gruneberg U, Nigg EA, Barr FA. Aurora B suppresses microtubule dynamics and limits central spindle size by locally activating KIF4A. J Cell Biol. 2013 Aug 19;202(4):605–21. doi: 10.1083/jcb.201301094 23940115

56. Gruneberg U, Neef R, Honda R, Nigg EA, Barr FA. Relocation of Aurora B from centromeres to the central spindle at the metaphase to anaphase transition requires MKlp2. The Journal of cell biology. 2004 Jul 19;166(2):167–72. doi: 10.1083/jcb.200403084 15263015

57. van Vugt MA, Medema RH. Getting in and out of mitosis with Polo-like kinase-1. Oncogene. 2005 Apr;24(17):2844. doi: 10.1038/sj.onc.1208617 15838519

58. Serio G, Margaria V, Jensen S, Oldani A, Bartek J, Bussolino F, Lanzetti L. Small GTPase Rab5 participates in chromosome congression and regulates localization of the centromere-associated protein CENP-F to kinetochores. Proceedings of the National Academy of Sciences. 2011 Oct 18;108(42):17337–42. doi: 10.1073/pnas.1103516108 21987812

59. Lénárt P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Current biology. 2007 Feb 20;17(4):304–15. doi: 10.1016/j.cub.2006.12.046 17291761

60. Sunkel CE, Glover DM. polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. Journal of cell science. 1988 Jan 1;89(1):25–38.

61. Corthésy-Theulaz I, Pauloin A, Pfeffer SR. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. The Journal of Cell Biology. 1992 Sep 15;118(6):1333–45. doi: 10.1083/jcb.118.6.1333 1387874

62. Kimura K, Kimura A. Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proceedings of the National Academy of Sciences. 2011 Jan 4;108(1):137–42. doi: 10.1073/pnas.1013275108 21173218

63. Yadav S, Linstedt AD. Golgi positioning. Cold Spring Harbor perspectives in biology. 2011 May 1;3(5):a005322. doi: 10.1101/cshperspect.a005322 21504874

64. Wang S, Romano FB, Field CM, Mitchison TJ, Rapoport TA. Multiple mechanisms determine ER network morphology during the cell cycle in Xenopus egg extracts. J Cell Biol. 2013 Dec 9;203(5):801–14. doi: 10.1083/jcb.201308001 24297752

65. Firestone AJ, Weinger JS, Maldonado M, Barlan K, Langston LD, O’donnell M, Gelfand VI, Kapoor TM, Chen JK. Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature. 2012 Apr;484(7392):125. doi: 10.1038/nature10936 22425997

66. Le Droguen PM, Claret S, Guichet A, Brodu V. Microtubule-dependent apical restriction of recycling endosomes sustains adherens junctions during morphogenesis of the Drosophila tracheal system. Development. 2015 Jan 15;142(2):363–74. doi: 10.1242/dev.113472 25564624

67. Sharp DJ. Rogers GC, Scholey JM. Microtubule motors in mitosis. Nature. 2000;407:41–7. doi: 10.1038/35024000 10993066

68. Smyth JT, Schoborg TA, Bergman ZJ, Riggs B, Rusan NM. Proper symmetric and asymmetric endoplasmic reticulum partitioning requires astral microtubules. Open biology. 2015 Aug 1;5(8):150067. doi: 10.1098/rsob.150067 26289801

69. Robinson JT, Wojcik EJ, Sanders MA, McGrail M, Hays TS. Cytoplasmic dynein is required for the nuclear attachment and migration of centrosomes during mitosis in Drosophila. The Journal of cell biology. 1999 Aug 9;146(3):597–608. doi: 10.1083/jcb.146.3.597 10444068

70. McGrail M, Hays TS. The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development. 1997 Jun 15;124(12):2409–19. 9199367

71. Wilde A, Zheng Y. Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran. Science. 1999 May 21;284(5418):1359–62. doi: 10.1126/science.284.5418.1359 10334991

72. English AR, Voeltz GK. Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harbor perspectives in biology. 2013 Apr 1;5(4):a013227. doi: 10.1101/cshperspect.a013227 23545422

73. Pina FJ, Niwa M. The ER Stress Surveillance (ERSU) pathway regulates daughter cell ER protein aggregate inheritance. Elife. 2015 Sep 1;4:e06970. doi: 10.7554/eLife.06970 26327697

74. Grigoriev I, Gouveia SM, Van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Current Biology. 2008 Feb 12;18(3):177–82. doi: 10.1016/j.cub.2007.12.050 18249114

75. Smyth JT, Beg AM, Wu S, Putney JW Jr, Rusan NM. Phosphoregulation of STIM1 leads to exclusion of the endoplasmic reticulum from the mitotic spindle. Current Biology. 2012 Aug 21;22(16):1487–93. doi: 10.1016/j.cub.2012.05.057 22748319

76. Bobinnec Y, Marcaillou C, Morin X, Debec A. Dynamics of the endoplasmic reticulum during early development of Drosophila melanogaster. Cell motility and the cytoskeleton. 2003 Mar;54(3):217–25. doi: 10.1002/cm.10094 12589680

77. Gurel PS, Hatch AL, Higgs HN. Connecting the cytoskeleton to the endoplasmic reticulum and Golgi. Current biology. 2014 Jul 21;24(14):R660–72. doi: 10.1016/j.cub.2014.05.033 25050967

78. Caviston JP, Holzbaur EL. Microtubule motors at the intersection of trafficking and transport. Trends in cell biology. 2006 Oct 1;16(10):530–7. doi: 10.1016/j.tcb.2006.08.002 16938456

79. Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell. 2002 Jan 11;108(1):97–107. doi: 10.1016/s0092-8674(01)00628-6 11792324

80. Bolhy S, Bouhlel I, Dultz E, Nayak T, Zuccolo M, Gatti X, Vallee R, Ellenberg J, Doye V. A Nup133-dependent NPC-anchored network tethers centrosomes to the nuclear envelope in prophase. The Journal of cell biology. 2011 Mar 7;192(5):855–71. doi: 10.1083/jcb.201007118 21383080

81. Karabasheva D., Smyth J.T. A novel, dynein-independent mechanism focuses the endoplasmic reticulum around spindle poles in dividing Drosophila spermatocytes. Sci Rep 9, 12456 (2019) doi: 10.1038/s41598-019-48860-4 31462700

82. Siegrist SE, Doe CQ. Microtubule-induced Pins/Gαi cortical polarity in Drosophila neuroblasts. Cell. 2005 Dec 29;123(7):1323–35. doi: 10.1016/j.cell.2005.09.043 16377571

83. Siller KH, Cabernard C, Doe CQ. The NuMA-related Mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nature cell biology. 2006 Jun;8(6):594. doi: 10.1038/ncb1412 16648843

84. Shibata Y, Voeltz GK, Rapoport TA. Rough sheets and smooth tubules. Cell. 2006 Aug 11;126(3):435–9. doi: 10.1016/j.cell.2006.07.019 16901774

85. Pendin D, McNew JA, Daga A. Balancing ER dynamics: shaping, bending, severing, and mending membranes. Current opinion in cell biology. 2011 Aug 1;23(4):435–42. doi: 10.1016/j.ceb.2011.04.007 21641197

86. Zurek N, Sparks L, Voeltz G. Reticulon short hairpin transmembrane domains are used to shape ER tubules. Traffic. 2011 Jan;12(1):28–41. doi: 10.1111/j.1600-0854.2010.01134.x 20955502

87. Schlaitz AL, Thompson J, Wong CC, Yates JR III, Heald R. REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Developmental cell. 2013 Aug 12;26(3):315–23. doi: 10.1016/j.devcel.2013.06.016 23911198

88. Park SH, Zhu PP, Parker RL, Blackstone C. Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. The Journal of clinical investigation. 2010 Apr 1;120(4):1097–110. doi: 10.1172/JCI40979 20200447

89. Mannan AU, Boehm J, Sauter SM, Rauber A, Byrne PC, Neesen J, Engel W. Spastin, the most commonly mutated protein in hereditary spastic paraplegia interacts with Reticulon 1 an endoplasmic reticulum protein. Neurogenetics. 2006 May 1;7(2):93. doi: 10.1007/s10048-006-0034-4 16602018

90. Allison R, Edgar JR, Pearson G, Rizo T, Newton T, Günther S, Berner F, Hague J, Connell JW, Winkler J, Lippincott-Schwartz J. Defects in ER–endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol. 2017 May 1;216(5):1337–55. doi: 10.1083/jcb.201609033 28389476

91. Jaqaman K, Danuser G. Linking data to models: data regression. Nature Reviews Molecular Cell Biology. 2006 Nov;7(11):813. doi: 10.1038/nrm2030 17006434

92. Horwitz R. Integrated, multi-scale, spatial–temporal cell biology–A next step in the post genomic era. Methods. 2016 Mar 1;96:3–5. doi: 10.1016/j.ymeth.2015.09.007 26361333

93. Carpenter AE. Image-based chemical screening. Nature Chemical Biology. 2007 Aug;3(8):461. doi: 10.1038/nchembio.2007.15 17637778


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