RAB-10-Dependent Membrane Transport Is Required for Dendrite Arborization

English version České info

Dendrites are cellular extensions from neurons that gather information from other neurons or cues from the external environment to convey to the nervous system of an organism. Dendrites are often extensively branched, raising the question of how neurons supply plasma membrane and dendrite specific proteins from the source of synthesis inside the cell to developing dendrites. We have examined membrane trafficking in the PVD neuron in the nematode worm C. elegans to investigate how new membrane and dendrite proteins are trafficked. The PVD neuron is easy to visualize and has remarkably long and widely branched dendrites positioned along the skin of the worm, which transmits information about harsh touch and cold temperature to the nervous system. We have discovered that a key organizer of vesicle trafficking, the RAB-10 protein, localizes to membrane vesicles and is required to traffic these vesicles that contain plasma membrane and dendrite proteins to the growing PVD dendrite. Further, our work revealed that a complex of proteins, termed the exocyst, that helps fuse membrane vesicles at the plasma membrane, localizes with RAB-10 and is required for dendrite branching. Together, our work has revealed a novel mechanism for how neurons build dendrites that could be used to help repair damaged neurons in human diseases and during aging.

Vyšlo v časopise: RAB-10-Dependent Membrane Transport Is Required for Dendrite Arborization. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005484
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005484

Souhrn

Zdroje

1. Ye B, Zhang Y, Song W, Younger SH, Jan LY, et al. (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130: 717–729. 17719548

2. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, et al. (2008) Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10: 1164–1171. doi: 10.1038/ncb1776 18758452

3. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R (2004) Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20: 87–123. 15473836

4. Lazo OM, Gonzalez A, Ascano M, Kuruvilla R, Couve A, et al. (2013) BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 33: 6112–6122. doi: 10.1523/JNEUROSCI.4630-12.2013 23554492

5. Way JC, Chalfie M (1989) The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev 3: 1823–1833. 2576011

6. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC, et al. (2010) Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 13: 861–868. doi: 10.1038/nn.2581 20512132

7. Li W, Kang L, Piggott BJ, Feng Z, Xu XZ (2011) The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun 2: 315. doi: 10.1038/ncomms1308 21587232

8. Smith CJ, Watson JD, Spencer WC, O'Brien T, Cha B, et al. (2010) Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev Biol 345: 18–33. doi: 10.1016/j.ydbio.2010.05.502 20537990

9. Liu OW, Shen K (2012) The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat Neurosci 15: 57–63.

10. Dong X, Liu OW, Howell AS, Shen K (2013) An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 155: 296–307. doi: 10.1016/j.cell.2013.08.059 24120131

11. Salzberg Y, Diaz-Balzac CA, Ramirez-Suarez NJ, Attreed M, Tecle E, et al. (2013) Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155: 308–320. doi: 10.1016/j.cell.2013.08.058 24120132

12. Smith CJ, O'Brien T, Chatzigeorgiou M, Spencer WC, Feingold-Link E, et al. (2013) Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization. Neuron 79: 266–280. doi: 10.1016/j.neuron.2013.05.009 23889932

13. Wang T, Liu Y, Xu XH, Deng CY, Wu KY, et al. (2011) Lgl1 activation of rab10 promotes axonal membrane trafficking underlying neuronal polarization. Dev Cell 21: 431–444. doi: 10.1016/j.devcel.2011.07.007 21856246

14. Liu Y, Xu XH, Chen Q, Wang T, Deng CY, et al. (2013) Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development. Nat Commun 4: 2005. doi: 10.1038/ncomms3005 23770993

15. Deng CY, Lei WL, Xu XH, Ju XC, Liu Y, et al. (2014) JIP1 mediates anterograde transport of Rab10 cargos during neuronal polarization. J Neurosci 34: 1710–1723. doi: 10.1523/JNEUROSCI.4496-13.2014 24478353

16. Xu XH, Deng CY, Liu Y, He M, Peng J, et al. (2014) MARCKS regulates membrane targeting of Rab10 vesicles to promote axon development. Cell Res 24: 576–594. doi: 10.1038/cr.2014.33 24662485

17. He B, Guo W (2009) The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21: 537–542. doi: 10.1016/j.ceb.2009.04.007 19473826

18. Frische EW, Pellis-van Berkel W, van Haaften G, Cuppen E, Plasterk RH, et al. (2007) RAP-1 and the RAL-1/exocyst pathway coordinate hypodermal cell organization in Caenorhabditis elegans. EMBO J 26: 5083–5092. 17989692

19. Babbey CM, Bacallao RL, Dunn KW (2010) Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 299: F495–506. doi: 10.1152/ajprenal.00198.2010 20576682

20. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, et al. (2007) Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5: 293–303. 17403373

21. Inoue M, Chang L, Hwang J, Chiang SH, Saltiel AR (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422: 629–633. 12687004

22. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, et al. (2006) Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17: 3156–3175. 16641372

23. Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, et al. (2007) Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8: 47–60. 17132146

24. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, et al. (2006) RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17: 1286–1297. 16394106

25. Glodowski DR, Chen CC, Schaefer H, Grant BD, Rongo C (2007) RAB-10 regulates glutamate receptor recycling in a cholesterol-dependent endocytosis pathway. Mol Biol Cell 18: 4387–4396. 17761527

26. Shi A, Chen CC, Banerjee R, Glodowski D, Audhya A, et al. (2010) EHBP-1 functions with RAB-10 during endocytic recycling in Caenorhabditis elegans. Mol Biol Cell 21: 2930–2943. doi: 10.1091/mbc.E10-02-0149 20573983

27. Arakawa H, Kudo H, Batrak V, Caldwell RB, Rieger MA, et al. (2008) Protein evolution by hypermutation and selection in the B cell line DT40. Nucleic Acids Res 36: e1. 18073192

28. Frokjaer-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, et al. (2014) Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nat Methods 11: 529–534. doi: 10.1038/nmeth.2889 24820376

29. Guo P, Hu T, Zhang J, Jiang S, Wang X (2010) Sequential action of Caenorhabditis elegans Rab GTPases regulates phagolysosome formation during apoptotic cell degradation. Proc Natl Acad Sci U S A 107: 18016–18021. doi: 10.1073/pnas.1008946107 20921409

30. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, et al. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 3: 573–579. 11389442

31. Chen B, Jiang Y, Zeng S, Yan J, Li X, et al. (2010) Endocytic sorting and recycling require membrane phosphatidylserine asymmetry maintained by TAT-1/CHAT-1. PLoS Genet 6: e1001235. doi: 10.1371/journal.pgen.1001235 21170358

32. Woodman PG (2000) Biogenesis of the sorting endosome: the role of Rab5. Traffic 1: 695–701. 11208157

33. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913–924. 8922376

34. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 103: 11821–11827. 16882731

35. Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18: 1071–1080. 10022848

36. Jiu Y, Jin C, Liu Y, Holmberg CI, Jantti J (2012) Exocyst subunits Exo70 and Exo84 cooperate with small GTPases to regulate behavior and endocytic trafficking in C. elegans. PLoS One 7: e32077. doi: 10.1371/journal.pone.0032077 22389680

37. Armenti ST, Lohmer LL, Sherwood DR, Nance J (2014) Repurposing an endogenous degradation system for rapid and targeted depletion of C. elegans proteins. Development 141: 4640–4647. doi: 10.1242/dev.115048 25377555

38. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, et al. (1998) Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93: 731–740. 9630218

39. Tsuboi T, Ravier MA, Xie H, Ewart MA, Gould GW, et al. (2005) Mammalian exocyst complex is required for the docking step of insulin vesicle exocytosis. J Biol Chem 280: 25565–25570. 15878854

40. Pereira-Leal JB, Seabra MC (2000) The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily. J Mol Biol 301: 1077–1087. 10966806

41. Shen Z, Zhang X, Chai Y, Zhu Z, Yi P, et al. (2014) Conditional knockouts generated by engineered CRISPR-Cas9 endonuclease reveal the roles of coronin in C. elegans neural development. Dev Cell 30: 625–636. doi: 10.1016/j.devcel.2014.07.017 25155554

42. Miyabayashi T, Palfreyman MT, Sluder AE, Slack F, Sengupta P (1999) Expression and function of members of a divergent nuclear receptor family in Caenorhabditis elegans. Dev Biol 215: 314–331. 10545240

43. Lerner DW, McCoy D, Isabella AJ, Mahowald AP, Gerlach GF, et al. (2013) A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 24: 159–168. doi: 10.1016/j.devcel.2012.12.005 23369713

44. Jones TA, Nikolova LS, Schjelderup A, Metzstein MM (2014) Exocyst-mediated membrane trafficking is required for branch outgrowth in Drosophila tracheal terminal cells. Dev Biol 390: 41–50. doi: 10.1016/j.ydbio.2014.02.021 24607370

45. Chen S, Li L, Li J, Liu B, Zhu X, et al. (2014) SEC-10 and RAB-10 coordinate basolateral recycling of clathrin-independent cargo through endosomal tubules in Caenorhabditis elegans. Proc Natl Acad Sci U S A 111: 15432–15437. doi: 10.1073/pnas.1408327111 25301900

46. Jiu Y, Hasygar K, Tang L, Liu Y, Holmberg CI, et al. (2014) par-1, atypical pkc, and PP2A/B55 sur-6 are implicated in the regulation of exocyst-mediated membrane trafficking in Caenorhabditis elegans. G3 (Bethesda) 4: 173–183.

47. Murthy M, Teodoro RO, Miller TP, Schwarz TL (2010) Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization. Development 137: 2773–2783. doi: 10.1242/dev.048330 20630948

48. Einstein G, Buranosky R, Crain BJ (1994) Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci 14: 5077–5088. 8046469

49. McNeill TH, Brown SA, Rafols JA, Shoulson I (1988) Atrophy of medium spiny I striatal dendrites in advanced Parkinson's disease. Brain Res 455: 148–152. 3416180

50. Aguirre-Chen C, Bulow HE, Kaprielian Z (2011) C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites. Development 138: 507–518. doi: 10.1242/dev.060939 21205795

51. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, et al. (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14: 2162–2168. 15489339

52. Inoue T, Sherwood DR, Aspock G, Butler JA, Gupta BP, et al. (2002) Gene expression markers for Caenorhabditis elegans vulval cells. Mech Dev 119 Suppl 1: S203–209. 14516686

53. Gallegos ME, Balakrishnan S, Chandramouli P, Arora S, Azameera A, et al. (2012) The C. elegans rab family: identification, classification and toolkit construction. PLoS One 7: e49387. doi: 10.1371/journal.pone.0049387 23185324

54. Hobert O (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32: 728–730. 11962590

55. Iyer EP, Iyer SC, Sullivan L, Wang D, Meduri R, et al. (2013) Functional genomic analyses of two morphologically distinct classes of Drosophila sensory neurons: post-mitotic roles of transcription factors in dendritic patterning. PLoS One 8: e72434. doi: 10.1371/journal.pone.0072434 23977298