The organization of Golgi in Drosophila bristles requires microtubule motor protein function and a properly organized microtubule array
Autoři:
Anna Melkov aff001; Raju Baskar aff001; Rotem Shachal aff001; Yehonathan Alcalay aff001; Uri Abdu aff001
Působiště autorů:
Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva, Israel
aff001
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223174
Souhrn
In the present report, we used highly elongated Drosophila bristle cells to dissect the role of dynein heavy chain (Dhc64C) in Golgi organization. We demonstrated that whereas in the bristle "somal" region Golgi units are composed of cis-, medial, and trans-Golgi compartments (“complete Golgi”), the bristle shaft contains Golgi satellites that lack the trans-Golgi compartment (hereafter referred to as “incomplete Golgi”) and which are static and localized at the base area. However, in Dhc64C mutants, the entire bristle shaft was filled with complete Golgi units containing ectopic trans-Golgi components. To further understand Golgi bristle organization, we tested the roles of microtubule (MT) polarity and the Dhc-opposing motor, kinesin heavy chain (Khc). For our surprise, we found that in Khc and Ik2Dominant-negative (DN) flies in which the polarized organization of MTs is affected, the bristle shaft was filled with complete Golgi, similarly to what is seen in Dhc64C flies. Thus, we demonstrated that MTs and the motor proteins Dhc and Khc are required for bristle Golgi organization. However, the fact that both Dhc64C and Khc flies showed similar Golgi defects calls for an additional work to elucidate the molecular mechanism describing why these factors are required for bristle Golgi organization.
Klíčová slova:
Actins – Cell staining – Cytoplasmic staining – Drosophila melanogaster – Neuronal dendrites – Golgi cells – Dyneins – Kinesins
Zdroje
1. Ayala I, Colanzi A. Alterations of Golgi organization in Alzheimer's disease: A cause or a consequence? Tissue Cell. 2017;49(2 Pt A):133–40. Epub 2016/11/30. doi: 10.1016/j.tice.2016.11.007 27894594.
2. van Vliet C, Thomas EC, Merino-Trigo A, Teasdale RD, Gleeson PA. Intracellular sorting and transport of proteins. Prog Biophys Mol Biol. 2003;83(1):1–45. Epub 2003/05/22. 12757749.
3. Klumperman J. Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol. 2011;3(7). Epub 2011/04/20. doi: 10.1101/cshperspect.a005181 21502307; PubMed Central PMCID: PMC3119909.
4. Marsh BJ, Mastronarde DN, Buttle KF, Howell KE, McIntosh JR. Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography. Proc Natl Acad Sci U S A. 2001;98(5):2399–406. Epub 2001/02/28. doi: 10.1073/pnas.051631998 11226251; PubMed Central PMCID: PMC30150.
5. Kondylis V, Rabouille C. The Golgi apparatus: lessons from Drosophila. FEBS Lett. 2009;583(23):3827–38. Epub 2009/10/06. doi: 10.1016/j.febslet.2009.09.048 19800333.
6. Aridor M, Guzik AK, Bielli A, Fish KN. Endoplasmic reticulum export site formation and function in dendrites. J Neurosci. 2004;24(15):3770–6. Epub 2004/04/16. doi: 10.1523/JNEUROSCI.4775-03.2004 15084657.
7. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell. 2007;130(4):717–29. Epub 2007/08/28. doi: 10.1016/j.cell.2007.06.032 17719548; PubMed Central PMCID: PMC2020851.
8. Horton AC, Ehlers MD. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci. 2003;23(15):6188–99. Epub 2003/07/18. doi: 10.1523/JNEUROSCI.23-15-06188.2003 12867502.
9. Hanus C, Ehlers MD. Secretory outposts for the local processing of membrane cargo in neuronal dendrites. Traffic. 2008;9(9):1437–45. Epub 2008/06/06. doi: 10.1111/j.1600-0854.2008.00775.x 18532987; PubMed Central PMCID: PMC2572994.
10. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, et al. The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell. 2001;12(7):2047–60. Epub 2001/07/14. doi: 10.1091/mbc.12.7.2047 11452002; PubMed Central PMCID: PMC55652.
11. Ori-McKenney KM, Jan LY, Jan YN. Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron. 2012;76(5):921–30. Epub 2012/12/12. doi: 10.1016/j.neuron.2012.10.008 PubMed Central PMCID: PMC3523279. 23217741
12. Nguyen MM, McCracken CJ, Milner ES, Goetschius DJ, Weiner AT, Long MK, et al. Gamma-tubulin controls neuronal microtubule polarity independently of Golgi outposts. Mol Biol Cell. 2014;25(13):2039–50. Epub 2014/05/09. doi: 10.1091/mbc.E13-09-0515 24807906; PubMed Central PMCID: PMC4072577.
13. Boulay AC, Saubamea B, Adam N, Chasseigneaux S, Mazare N, Gilbert A, et al. Translation in astrocyte distal processes sets molecular heterogeneity at the gliovascular interface. Cell Discov. 2017;3:17005. Epub 2017/04/06. doi: 10.1038/celldisc.2017.5 28377822; PubMed Central PMCID: PMC5368712.
14. Hanus C, Ehlers MD. Specialization of biosynthetic membrane trafficking for neuronal form and function. Curr Opin Neurobiol. 2016;39:8–16. Epub 2016/03/25. doi: 10.1016/j.conb.2016.03.004 27010827.
15. Bitan A, Rosenbaum I, Abdu U. Stable and dynamic microtubules coordinately determine and maintain Drosophila bristle shape. Development. 2012;139(11):1987–96. Epub 2012/04/20. doi: 10.1242/dev.076893 22513371.
16. Melkov A, Abdu U. Regulation of long-distance transport of mitochondria along microtubules. Cell Mol Life Sci. 2018;75(2):163–76. Epub 2017/07/14. doi: 10.1007/s00018-017-2590-1 28702760.
17. Melkov A, Baskar R, Alcalay Y, Abdu U. A new mode of mitochondrial transport and polarized sorting regulated by Dynein, Milton and Miro. Development. 2016;143(22):4203–13. Epub 2016/11/02. doi: 10.1242/dev.138289 27707795.
18. Melkov A, Simchoni Y, Alcalay Y, Abdu U. Dynamic microtubule organization and mitochondrial transport are regulated by distinct Kinesin-1 pathways. Biol Open. 2015;4(12):1696–706. Epub 2015/11/20. doi: 10.1242/bio.015206 26581590; PubMed Central PMCID: PMC4736040.
19. Nagaraj R, Adler PN. Dusky-like functions as a Rab11 effector for the deposition of cuticle during Drosophila bristle development. Development. 2012;139(5):906–16. Epub 2012/01/27. doi: 10.1242/dev.074252 22278919; PubMed Central PMCID: PMC3274354.
20. Gepner J, Li M, Ludmann S, Kortas C, Boylan K, Iyadurai SJ, et al. Cytoplasmic dynein function is essential in Drosophila melanogaster. Genetics. 1996;142(3):865–78. Epub 1996/03/01. 8849893; PubMed Central PMCID: PMC1207024.
21. Li Z, Wang L, Hays TS, Cai Y. Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity. J Cell Biol. 2008;180(1):31–8. Epub 2008/01/16. doi: 10.1083/jcb.200707007 18195099; PubMed Central PMCID: PMC2213619.
22. Oshima K, Takeda M, Kuranaga E, Ueda R, Aigaki T, Miura M, et al. IKK epsilon regulates F actin assembly and interacts with Drosophila IAP1 in cellular morphogenesis. Curr Biol. 2006;16(15):1531–7. Epub 2006/08/05. doi: 10.1016/j.cub.2006.06.032 16887350.
23. Zhou W, Chang J, Wang X, Savelieff MG, Zhao Y, Ke S, et al. GM130 is required for compartmental organization of dendritic golgi outposts. Curr Biol. 2014;24(11):1227–33. Epub 2014/05/20. doi: 10.1016/j.cub.2014.04.008 24835455; PubMed Central PMCID: PMC4047983.
24. Forster D, Armbruster K, Luschnig S. Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Current biology: CB. 2010;20(1):62–8. doi: 10.1016/j.cub.2009.11.062 20045324.
25. Guild GM, Connelly PS, Vranich KA, Shaw MK, Tilney LG. Actin filament turnover removes bundles from Drosophila bristle cells. J Cell Sci. 2002;115(Pt 3):641–53. Epub 2002/02/28. 11861770.
26. Ivan V, de Voer G, Xanthakis D, Spoorendonk KM, Kondylis V, Rabouille C. Drosophila Sec16 mediates the biogenesis of tER sites upstream of Sar1 through an arginine-rich motif. Mol Biol Cell. 2008;19(10):4352–65. Epub 2008/07/11. doi: 10.1091/mbc.E08-03-0246 18614796; PubMed Central PMCID: PMC2555954.
27. Kondylis V, Goulding SE, Dunne JC, Rabouille C. Biogenesis of Golgi stacks in imaginal discs of Drosophila melanogaster. Molecular biology of the cell. 2001;12(8):2308–27. doi: 10.1091/mbc.12.8.2308 11514618; PubMed Central PMCID: PMC58596.
28. Yano H, Yamamoto-Hino M, Abe M, Kuwahara R, Haraguchi S, Kusaka I, et al. Distinct functional units of the Golgi complex in Drosophila cells. Proc Natl Acad Sci U S A. 2005;102(38):13467–72. Epub 2005/09/22. doi: 10.1073/pnas.0506681102 16174741; PubMed Central PMCID: PMC1224666.
29. Rabouille C, Kuntz DA, Lockyer A, Watson R, Signorelli T, Rose DR, et al. The Drosophila GMII gene encodes a Golgi alpha-mannosidase II. J Cell Sci. 1999;112 (Pt 19):3319–30. Epub 1999/10/03. 10504337.
30. Mackenzie JM, Jones MK, Westaway EG. Markers for trans-Golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells. J Virol. 1999;73(11):9555–67. Epub 1999/10/09. 10516064; PubMed Central PMCID: PMC112990.
31. Yadav S, Linstedt AD. Golgi positioning. Cold Spring Harb Perspect Biol. 2011;3(5). Epub 2011/04/21. doi: 10.1101/cshperspect.a005322 21504874; PubMed Central PMCID: PMC3101843.
32. Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, Hirokawa N. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol. 1998;141(1):51–9. Epub 1998/05/16. doi: 10.1083/jcb.141.1.51 9531547; PubMed Central PMCID: PMC2132725.
33. Corthesy-Theulaz I, Pauloin A, Pfeffer SR. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol. 1992;118(6):1333–45. Epub 1992/09/01. doi: 10.1083/jcb.118.6.1333 1387874; PubMed Central PMCID: PMC2289611.
34. Vallee RB, Williams JC, Varma D, Barnhart LE. Dynein: An ancient motor protein involved in multiple modes of transport. J Neurobiol. 2004;58(2):189–200. Epub 2004/01/06. doi: 10.1002/neu.10314 14704951.
35. Sisson JC, Field C, Ventura R, Royou A, Sullivan W. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J Cell Biol. 2000;151(4):905–18. Epub 2000/11/15. doi: 10.1083/jcb.151.4.905 11076973; PubMed Central PMCID: PMC2169433.
36. Papoulas O, Hays TS, Sisson JC. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat Cell Biol. 2005;7(6):612–8. Epub 2005/05/24. doi: 10.1038/ncb1264 15908943.
37. Lin CH, Li H, Lee YN, Cheng YJ, Wu RM, Chien CT. Lrrk regulates the dynamic profile of dendritic Golgi outposts through the golgin Lava lamp. J Cell Biol. 2015;210(3):471–83. Epub 2015/07/29. doi: 10.1083/jcb.201411033 26216903; PubMed Central PMCID: PMC4523617.
38. Gyoeva FK, Bybikova EM, Minin AA. An isoform of kinesin light chain specific for the Golgi complex. J Cell Sci. 2000;113 (Pt 11):2047–54. Epub 2000/05/12. 10806115.
39. Dubin-Bar D, Bitan A, Bakhrat A, Kaiden-Hasson R, Etzion S, Shaanan B, et al. The Drosophila IKK-related kinase (Ik2) and Spindle-F proteins are part of a complex that regulates cytoskeleton organization during oogenesis. BMC Cell Biol. 2008;9:51. Epub 2008/09/18. doi: 10.1186/1471-2121-9-51 18796167; PubMed Central PMCID: PMC2567969.
40. Shapiro RS, Anderson KV. Drosophila Ik2, a member of the I kappa B kinase family, is required for mRNA localization during oogenesis. Development. 2006;133(8):1467–75. Epub 2006/03/17. doi: 10.1242/dev.02318 16540511.
41. Otani T, Oshima K, Onishi S, Takeda M, Shinmyozu K, Yonemura S, et al. IKKepsilon regulates cell elongation through recycling endosome shuttling. Dev Cell. 2011;20(2):219–32. Epub 2011/02/15. doi: 10.1016/j.devcel.2011.02.001 21316589.
42. Farkas RM, Giansanti MG, Gatti M, Fuller MT. The Drosophila Cog5 homologue is required for cytokinesis, cell elongation, and assembly of specialized Golgi architecture during spermatogenesis. Mol Biol Cell. 2003;14(1):190–200. Epub 2003/01/17. doi: 10.1091/mbc.E02-06-0343 12529436; PubMed Central PMCID: PMC140237.
43. Fari K, Takacs S, Ungar D, Sinka R. The role of acroblast formation during Drosophila spermatogenesis. Biol Open. 2016;5(8):1102–10. Epub 2016/08/03. doi: 10.1242/bio.018275 27481842; PubMed Central PMCID: PMC5004609.
44. Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron. 2005;48(5):757–71. Epub 2005/12/13. doi: 10.1016/j.neuron.2005.11.005 16337914.
45. Baas PW, Deitch JS, Black MM, Banker GA. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc Natl Acad Sci U S A. 1988;85(21):8335–9. Epub 1988/11/01. doi: 10.1073/pnas.85.21.8335 3054884; PubMed Central PMCID: PMC282424.
46. Stone MC, Roegiers F, Rolls MM. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell. 2008;19(10):4122–9. Epub 2008/08/01. doi: 10.1091/mbc.E07-10-1079 18667536; PubMed Central PMCID: PMC2555934.
47. Nakata T, Hirokawa N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol. 2003;162(6):1045–55. Epub 2003/09/17. doi: 10.1083/jcb.200302175 12975348; PubMed Central PMCID: PMC2172855.
48. Cole NB, Sciaky N, Marotta A, Song J, Lippincott-Schwartz J. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol Biol Cell. 1996;7(4):631–50. Epub 1996/04/01. doi: 10.1091/mbc.7.4.631 8730104; PubMed Central PMCID: PMC275914.
49. Ho WC, Allan VJ, van Meer G, Berger EG, Kreis TE. Reclustering of scattered Golgi elements occurs along microtubules. Eur J Cell Biol. 1989;48(2):250–63. Epub 1989/04/01. 2743999.
50. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A, Younger SH, et al. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat Cell Biol. 2008;10(10):1172–80. Epub 2008/09/02. doi: 10.1038/ncb1777 18758451; PubMed Central PMCID: PMC2588425.
51. Kelliher MT, Yue Y, Ng A, Kamiyama D, Huang B, Verhey KJ, et al. Autoinhibition of kinesin-1 is essential to the dendrite-specific localization of Golgi outposts. The Journal of cell biology. 2018. doi: 10.1083/jcb.201708096 29728423.
Článek vyšel v časopise
PLOS One
2019 Číslo 10
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy